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1. Hyperactive nanobacteria with host-dependent traits pervade Omnitrophota

Author

Seymour, Cale O, Palmer, Marike, Becraft, Eric D, Stepanauskas, Ramunas, Friel, Ariel D, Schulz, Frederik, Woyke, Tanja, Eloe-Fadrosh, Emiley, Lai, Dengxun, Jiao, Jian-Yu, Hua, Zheng-Shuang, Liu, Lan, Lian, Zheng-Han, Li, Wen-Jun, Chuvochina, Maria, Finley, Brianna K, Koch, Benjamin J, Schwartz, Egbert, Dijkstra, Paul, Moser, Duane P, Hungate, Bruce A, and Hedlund, Brian P

Subjects
Biological Sciences, Ecology, Humans, Calcifying Nanoparticles, Bacteria, Microbiota, Microbiology, Medical Microbiology
Abstract

Candidate bacterial phylum Omnitrophota has not been isolated and is poorly understood. We analysed 72 newly sequenced and 349 existing Omnitrophota genomes representing 6 classes and 276 species, along with Earth Microbiome Project data to evaluate habitat, metabolic traits and lifestyles. We applied fluorescence-activated cell sorting and differential size filtration, and showed that most Omnitrophota are ultra-small (~0.2 μm) cells that are found in water, sediments and soils. Omnitrophota genomes in 6 classes are reduced, but maintain major biosynthetic and energy conservation pathways, including acetogenesis (with or without the Wood-Ljungdahl pathway) and diverse respirations. At least 64% of Omnitrophota genomes encode gene clusters typical of bacterial symbionts, suggesting host-associated lifestyles. We repurposed quantitative stable-isotope probing data from soils dominated by andesite, basalt or granite weathering and identified 3 families with high isotope uptake consistent with obligate bacterial predators. We propose that most Omnitrophota inhabit various ecosystems as predators or parasites.

Published
2023

2. Synthase-Selective Exploration of a Tunicate Microbiome by Activity-Guided Single-Cell Genomics

Author

Kim, Woojoo E, Charov, Katherine, Džunková, Mária, Becraft, Eric D, Brown, Julia, Schulz, Frederik, Woyke, Tanja, La Clair, James J, Stepanauskas, Ramunas, and Burkart, Michael D

Subjects
Microbiology, Biochemistry and Cell Biology, Biological Sciences, Microbiome, Human Genome, Genetics, Biotechnology, Animals, Bacillus subtilis, Carrier Proteins, Ciona intestinalis, Computational Biology, Escherichia coli, Flow Cytometry, Genomics, Microbiota, Multigene Family, Peptide Synthases, Phylogeny, Polyketides, Secondary Metabolism, Siderophores, Single-Cell Analysis, Chemical Sciences, Organic Chemistry, Biological sciences, Chemical sciences
Abstract

While thousands of environmental metagenomes have been mined for the presence of novel biosynthetic gene clusters, such computational predictions do not provide evidence of their in vivo biosynthetic functionality. Using fluorescent in situ enzyme assay targeting carrier proteins common to polyketide (PKS) and nonribosomal peptide synthetases (NRPS), we applied fluorescence-activated cell sorting to tunicate microbiome to enrich for microbes with active secondary metabolic capabilities. Single-cell genomics uncovered the genetic basis for a wide biosynthetic diversity in the enzyme-active cells and revealed a member of marine Oceanospirillales harboring a novel NRPS gene cluster with high similarity to phylogenetically distant marine and terrestrial bacteria. Interestingly, this synthase belongs to a larger class of siderophore biosynthetic gene clusters commonly associated with pestilence and disease. This demonstrates activity-guided single-cell genomics as a tool to guide novel biosynthetic discovery.

Published
2021

3. Hiding in Plain Sight: The Globally Distributed Bacterial Candidate Phylum PAUC34f

Author

Chen, Michael L, Becraft, Eric D, Pachiadaki, Maria, Brown, Julia M, Jarett, Jessica K, Gasol, Josep M, Ravin, Nikolai V, Moser, Duane P, Nunoura, Takuro, Herndl, Gerhard J, Woyke, Tanja, and Stepanauskas, Ramunas

Subjects
Microbiology, Biological Sciences, Ecology, Life Below Water, microbial ecology, uncultivated bacteria, microbial genomics, dark ocean, host-association, Environmental Science and Management, Soil Sciences, Medical microbiology
Abstract

Bacterial candidate phylum PAUC34f was originally discovered in marine sponges and is widely considered to be composed of sponge symbionts. Here, we report 21 single amplified genomes (SAGs) of PAUC34f from a variety of environments, including the dark ocean, lake sediments, and a terrestrial aquifer. The diverse origins of the SAGs and the results of metagenome fragment recruitment suggest that some PAUC34f lineages represent relatively abundant, free-living cells in environments other than sponge microbiomes, including the deep ocean. Both phylogenetic and biogeographic patterns, as well as genome content analyses suggest that PAUC34f associations with hosts evolved independently multiple times, while free-living lineages of PAUC34f are distinct and relatively abundant in a wide range of environments.

Published
2020

4. Ancestral Absence of Electron Transport Chains in Patescibacteria and DPANN

Author

Beam, Jacob P, Becraft, Eric D, Brown, Julia M, Schulz, Frederik, Jarett, Jessica K, Bezuidt, Oliver, Poulton, Nicole J, Clark, Kayla, Dunfield, Peter F, Ravin, Nikolai V, Spear, John R, Hedlund, Brian P, Kormas, Konstantinos A, Sievert, Stefan M, Elshahed, Mostafa S, Barton, Hazel A, Stott, Matthew B, Eisen, Jonathan A, Moser, Duane P, Onstott, Tullis C, Woyke, Tanja, and Stepanauskas, Ramunas

Subjects
Microbiology, Biological Sciences, Human Genome, Genetics, Generic health relevance, Bacteria, Archaea, evolution, genomics fermentation, respiration, oxidoreductases, Environmental Science and Management, Soil Sciences, Medical microbiology
Abstract

Recent discoveries suggest that the candidate superphyla Patescibacteria and DPANN constitute a large fraction of the phylogenetic diversity of Bacteria and Archaea. Their small genomes and limited coding potential have been hypothesized to be ancestral adaptations to obligate symbiotic lifestyles. To test this hypothesis, we performed cell-cell association, genomic, and phylogenetic analyses on 4,829 individual cells of Bacteria and Archaea from 46 globally distributed surface and subsurface field samples. This confirmed the ubiquity and abundance of Patescibacteria and DPANN in subsurface environments, the small size of their genomes and cells, and the divergence of their gene content from other Bacteria and Archaea. Our analyses suggest that most Patescibacteria and DPANN in the studied subsurface environments do not form specific physical associations with other microorganisms. These data also suggest that their unusual genomic features and prevalent auxotrophies may be a result of ancestral, minimal cellular energy transduction mechanisms that lack respiration, thus relying solely on fermentation for energy conservation.

Published
2020

5. Author Correction: Hydrogen-based metabolism as an ancestral trait in lineages sibling to the Cyanobacteria.

Author

Matheus Carnevali, Paula B, Schulz, Frederik, Castelle, Cindy J, Kantor, Rose S, Shih, Patrick M, Sharon, Itai, Santini, Joanne M, Olm, Matthew R, Amano, Yuki, Thomas, Brian C, Anantharaman, Karthik, Burstein, David, Becraft, Eric D, Stepanauskas, Ramunas, Woyke, Tanja, and Banfield, Jillian F

Abstract

The original version of this Article contained errors in Fig. 4. In panel a, the labels 'F420-reducing NiFe hydrogenase (group 3a)' and 'Group 2 NiFe hydrogenase' were misplaced. These errors have been corrected in both the PDF and HTML versions of the Article.

Published
2019

6. Four Draft Single-Cell Genome Sequences of Novel, Nearly Identical Kiritimatiellaeota Strains Isolated from the Continental Deep Subsurface.

Author

Sackett, Joshua D, Kruger, Brittany R, Becraft, Eric D, Jarett, Jessica K, Stepanauskas, Ramunas, Woyke, Tanja, and Moser, Duane P

Abstract

The recently proposed bacterial phylum Kiritimatiellaeota represents a globally distributed monophyletic clade distinct from other members of the Planctomycetes, Verrucomicrobia, and Chlamydiae (PVC) superphylum. Here, we present four phylogenetically distinct single-cell genome sequences from within the Kiritimatiellaeota lineage sampled from deep continental subsurface aquifer fluids of the Death Valley Regional Flow System in the United States.

Published
2019

7. Hydrogen-based metabolism as an ancestral trait in lineages sibling to the Cyanobacteria.

Author

Matheus Carnevali, Paula B, Schulz, Frederik, Castelle, Cindy J, Kantor, Rose S, Shih, Patrick M, Sharon, Itai, Santini, Joanne M, Olm, Matthew R, Amano, Yuki, Thomas, Brian C, Anantharaman, Karthik, Burstein, David, Becraft, Eric D, Stepanauskas, Ramunas, Woyke, Tanja, and Banfield, Jillian F

Subjects
Cyanobacteria, Oxygen, Hydrogen, Hydrogenase, Nitrogenase, Bacterial Proteins, Sequence Analysis, DNA, Phylogeny, Species Specificity, Aerobiosis, Anaerobiosis, Fermentation, Oxidation-Reduction, Genome, Bacterial, Sequence Analysis, DNA, Genome, Bacterial, MD Multidisciplinary
Abstract

The evolution of aerobic respiration was likely linked to the origins of oxygenic Cyanobacteria. Close phylogenetic neighbors to Cyanobacteria, such as Margulisbacteria (RBX-1 and ZB3), Saganbacteria (WOR-1), Melainabacteria and Sericytochromatia, may constrain the metabolic platform in which aerobic respiration arose. Here, we analyze genomic sequences and predict that sediment-associated Margulisbacteria have a fermentation-based metabolism featuring a variety of hydrogenases, a streamlined nitrogenase, and electron bifurcating complexes involved in cycling of reducing equivalents. The genomes of ocean-associated Margulisbacteria encode an electron transport chain that may support aerobic growth. Some Saganbacteria genomes encode various hydrogenases, and others may be able to use O2 under certain conditions via a putative novel type of heme copper O2 reductase. Similarly, Melainabacteria have diverse energy metabolisms and are capable of fermentation and aerobic or anaerobic respiration. The ancestor of all these groups may have been an anaerobe in which fermentation and H2 metabolism were central metabolic features. The ability to use O2 as a terminal electron acceptor must have been subsequently acquired by these lineages.

Published
2019

8. Corrigendum: Minimum information about a single amplified genome (MISAG) and a metagenome-assembled genome (MIMAG) of bacteria and archaea.

Author

Bowers, Robert M, Kyrpides, Nikos C, Stepanauskas, Ramunas, Harmon-Smith, Miranda, Doud, Devin, Reddy, TBK, Schulz, Frederik, Jarett, Jessica, Rivers, Adam R, Eloe-Fadrosh, Emiley A, Tringe, Susannah G, Ivanova, Natalia N, Copeland, Alex, Clum, Alicia, Becraft, Eric D, Malmstrom, Rex R, Birren, Bruce, Podar, Mircea, Bork, Peer, Weinstock, George M, Garrity, George M, Dodsworth, Jeremy A, Yooseph, Shibu, Sutton, Granger, Glöckner, Frank O, Gilbert, Jack A, Nelson, William C, Hallam, Steven J, Jungbluth, Sean P, Ettema, Thijs JG, Tighe, Scott, Konstantinidis, Konstantinos T, Liu, Wen-Tso, Baker, Brett J, Rattei, Thomas, Eisen, Jonathan A, Hedlund, Brian, McMahon, Katherine D, Fierer, Noah, Knight, Rob, Finn, Rob, Cochrane, Guy, Karsch-Mizrachi, Ilene, Tyson, Gene W, Rinke, Christian, Genome Standards Consortium, Lapidus, Alla, Meyer, Folker, Yilmaz, Pelin, Parks, Donovan H, Eren, AM, Schriml, Lynn, Banfield, Jillian F, Hugenholtz, Philip, and Woyke, Tanja

Subjects
Genome Standards Consortium
Abstract

In the version of this article initially published, the author A. Murat Eren was listed as A.M. Eren. The corresponding affiliation was given as the Knapp Center for Biomedical Discovery, rather than Department of Medicine, University of Chicago, Chicago, Illinois, USA, and Marine Biological Laboratory, Woods Hole, Massachusetts, USA. The errors have been corrected in the HTML and PDF versions of the article as of 29 November 2017. In the version of this article initially published, the following acknowledgment was omitted: A.L. was supported by the Russian Science Foundation (grant number 14-50-00069). The error has been corrected in the HTML and PDF versions of the article as of 7 December 2017.

Published
2018

9. Correction: Corrigendum: Minimum information about a single amplified genome (MISAG) and a metagenome-assembled genome (MIMAG) of bacteria and archaea

Author

Bowers, Robert M, Kyrpides, Nikos C, Stepanauskas, Ramunas, Harmon-Smith, Miranda, Doud, Devin, Reddy, TBK, Schulz, Frederik, Jarett, Jessica, Rivers, Adam R, Eloe-Fadrosh, Emiley A, Tringe, Susannah G, Ivanova, Natalia N, Copeland, Alex, Clum, Alicia, Becraft, Eric D, Malmstrom, Rex R, Birren, Bruce, Podar, Mircea, Bork, Peer, Weinstock, George M, Garrity, George M, Dodsworth, Jeremy A, Yooseph, Shibu, Sutton, Granger, Glöckner, Frank O, Gilbert, Jack A, Nelson, William C, Hallam, Steven J, Jungbluth, Sean P, Ettema, Thijs JG, Tighe, Scott, Konstantinidis, Konstantinos T, Liu, Wen-Tso, Baker, Brett J, Rattei, Thomas, Eisen, Jonathan A, Hedlund, Brian, McMahon, Katherine D, Fierer, Noah, Knight, Rob, Finn, Rob, Cochrane, Guy, Karsch-Mizrachi, Ilene, Tyson, Gene W, Rinke, Christian, Lapidus, Alla, Meyer, Folker, Yilmaz, Pelin, Parks, Donovan H, Eren, A Murat, Schriml, Lynn, Banfield, Jillian F, Hugenholtz, Philip, and Woyke, Tanja

Subjects
Biological Sciences, Genetics, Genome Standards Consortium
Published
2018

10. Minimum information about a single amplified genome (MISAG) and a metagenome-assembled genome (MIMAG) of bacteria and archaea

Author

Bowers, Robert M, Kyrpides, Nikos C, Stepanauskas, Ramunas, Harmon-Smith, Miranda, Doud, Devin, Reddy, TBK, Schulz, Frederik, Jarett, Jessica, Rivers, Adam R, Eloe-Fadrosh, Emiley A, Tringe, Susannah G, Ivanova, Natalia N, Copeland, Alex, Clum, Alicia, Becraft, Eric D, Malmstrom, Rex R, Birren, Bruce, Podar, Mircea, Bork, Peer, Weinstock, George M, Garrity, George M, Dodsworth, Jeremy A, Yooseph, Shibu, Sutton, Granger, Glöckner, Frank O, Gilbert, Jack A, Nelson, William C, Hallam, Steven J, Jungbluth, Sean P, Ettema, Thijs JG, Tighe, Scott, Konstantinidis, Konstantinos T, Liu, Wen-Tso, Baker, Brett J, Rattei, Thomas, Eisen, Jonathan A, Hedlund, Brian, McMahon, Katherine D, Fierer, Noah, Knight, Rob, Finn, Rob, Cochrane, Guy, Karsch-Mizrachi, Ilene, Tyson, Gene W, Rinke, Christian, Lapidus, Alla, Meyer, Folker, Yilmaz, Pelin, Parks, Donovan H, Murat Eren, A, Schriml, Lynn, Banfield, Jillian F, Hugenholtz, Philip, and Woyke, Tanja

Subjects
Microbiology, Biological Sciences, Bioinformatics and Computational Biology, Genetics, Cancer, Cancer Genomics, Biotechnology, Human Genome, Genome, Archaeal, Genome, Bacterial, Genomics, Metagenomics, Sequence Analysis, DNA, Genome Standards Consortium
Abstract

We present two standards developed by the Genomic Standards Consortium (GSC) for reporting bacterial and archaeal genome sequences. Both are extensions of the Minimum Information about Any (x) Sequence (MIxS). The standards are the Minimum Information about a Single Amplified Genome (MISAG) and the Minimum Information about a Metagenome-Assembled Genome (MIMAG), including, but not limited to, assembly quality, and estimates of genome completeness and contamination. These standards can be used in combination with other GSC checklists, including the Minimum Information about a Genome Sequence (MIGS), Minimum Information about a Metagenomic Sequence (MIMS), and Minimum Information about a Marker Gene Sequence (MIMARKS). Community-wide adoption of MISAG and MIMAG will facilitate more robust comparative genomic analyses of bacterial and archaeal diversity.

Published
2017

11. Evolutionary stasis of a deep subsurface microbial lineage

Author

Becraft, Eric D., Lau Vetter, Maggie C. Y., Bezuidt, Oliver K. I., Brown, Julia M., Labonté, Jessica M., Kauneckaite-Griguole, Kotryna, Salkauskaite, Ruta, Alzbutas, Gediminas, Sackett, Joshua D., Kruger, Brittany R., Kadnikov, Vitaly, van Heerden, Esta, Moser, Duane, Ravin, Nikolai, Onstott, Tullis, and Stepanauskas, Ramunas

Published
2021
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12. Rokubacteria: Genomic Giants among the Uncultured Bacterial Phyla

Author

Becraft, Eric D, Woyke, Tanja, Jarett, Jessica, Ivanova, Natalia, Godoy-Vitorino, Filipa, Poulton, Nicole, Brown, Julia M, Brown, Joseph, Lau, MCY, Onstott, Tullis, Eisen, Jonathan A, Moser, Duane, and Stepanauskas, Ramunas

Subjects
Genetics, Biotechnology, Human Genome, Life Below Water, microbial ecology, microbial evolution, uncultivated bacteria, microbial dark matter, microbial genomics, Environmental Science and Management, Soil Sciences, Microbiology
Abstract

Recent advances in single-cell genomic and metagenomic techniques have facilitated the discovery of numerous previously unknown, deep branches of the tree of life that lack cultured representatives. Many of these candidate phyla are composed of microorganisms with minimalistic, streamlined genomes lacking some core metabolic pathways, which may contribute to their resistance to growth in pure culture. Here we analyzed single-cell genomes and metagenome bins to show that the "Candidate phylum Rokubacteria," formerly known as SPAM, represents an interesting exception, by having large genomes (6-8 Mbps), high GC content (66-71%), and the potential for a versatile, mixotrophic metabolism. We also observed an unusually high genomic heterogeneity among individual Rokubacteria cells in the studied samples. These features may have contributed to the limited recovery of sequences of this candidate phylum in prior cultivation and metagenomic studies. Our analyses suggest that Rokubacteria are distributed globally in diverse terrestrial ecosystems, including soils, the rhizosphere, volcanic mud, oil wells, aquifers, and the deep subsurface, with no reports from marine environments to date.

Published
2017

15. A genomic catalog of Earth’s microbiomes

Author

Nayfach, Stephen, Roux, Simon, Seshadri, Rekha, Udwary, Daniel, Varghese, Neha, Schulz, Frederik, Wu, Dongying, Paez-Espino, David, Chen, I. Min, Huntemann, Marcel, Palaniappan, Krishna, Ladau, Joshua, Mukherjee, Supratim, Reddy, T. B.K., Nielsen, Torben, Kirton, Edward, Faria, José P., Edirisinghe, Janaka N., Henry, Christopher S., Jungbluth, Sean P., Chivian, Dylan, Dehal, Paramvir, Wood-Charlson, Elisha M., Arkin, Adam P., Tringe, Susannah G., Visel, Axel, Abreu, Helena, Acinas, Silvia G., Allen, Eric, Allen, Michelle A., Alteio, Lauren V., Andersen, Gary, Anesio, Alexandre M., Attwood, Graeme, Avila-Magaña, Viridiana, Badis, Yacine, Bailey, Jake, Baker, Brett, Baldrian, Petr, Barton, Hazel A., Beck, David A.C., Becraft, Eric D., Beller, Harry R., Beman, J. Michael, Bernier-Latmani, Rizlan, Berry, Timothy D., Bertagnolli, Anthony, Bertilsson, Stefan, Bhatnagar, Jennifer M., Bird, Jordan T., Blanchard, Jeffrey L., Blumer-Schuette, Sara E., Bohannan, Brendan, Borton, Mikayla A., Brady, Allyson, Brawley, Susan H., Brodie, Juliet, Brown, Steven, Brum, Jennifer R., Brune, Andreas, Bryant, Donald A., Buchan, Alison, Buckley, Daniel H., Buongiorno, Joy, Cadillo-Quiroz, Hinsby, Caffrey, Sean M., Campbell, Ashley N., Campbell, Barbara, Carr, Stephanie, Carroll, Jo Lynn, Cary, S. Craig, Cates, Anna M., Cattolico, Rose Ann, Cavicchioli, Ricardo, Chistoserdova, Ludmila, Coleman, Maureen L., Constant, Philippe, Conway, Jonathan M., Mac Cormack, Walter P., Crowe, Sean, Crump, Byron, Currie, Cameron, Daly, Rebecca, DeAngelis, Kristen M., Denef, Vincent, Denman, Stuart E., Desta, Adey, Dionisi, Hebe, Dodsworth, Jeremy, Dombrowski, Nina, Donohue, Timothy, Dopson, Mark, Driscoll, Timothy, Dunfield, Peter, Dupont, Christopher L., Dynarski, Katherine A., Edgcomb, Virginia, Edwards, Elizabeth A., Elshahed, Mostafa S., Figueroa, Israel, Flood, Beverly, Fortney, Nathaniel, Fortunato, Caroline S., Francis, Christopher, Gachon, Claire M.M., Garcia, Sarahi L., Gazitua, Maria C., Gentry, Terry, Gerwick, Lena, Gharechahi, Javad, Girguis, Peter, Gladden, John, Gradoville, Mary, Grasby, Stephen E., Gravuer, Kelly, Grettenberger, Christen L., Gruninger, Robert J., Guo, Jiarong, Habteselassie, Mussie Y., Hallam, Steven J., Hatzenpichler, Roland, Hausmann, Bela, Hazen, Terry C., Hedlund, Brian, Henny, Cynthia, Herfort, Lydie, Hernandez, Maria, Hershey, Olivia S., Hess, Matthias, Hollister, Emily B., Hug, Laura A., Hunt, Dana, Jansson, Janet, Jarett, Jessica, Kadnikov, Vitaly V., Kelly, Charlene, Kelly, Robert, Kelly, William, Kerfeld, Cheryl A., Kimbrel, Jeff, Klassen, Jonathan L., Konstantinidis, Konstantinos T., Lee, Laura L., Li, Wen Jun, Loder, Andrew J., Loy, Alexander, Lozada, Mariana, MacGregor, Barbara, Magnabosco, Cara, Maria da Silva, Aline, McKay, R. Michael, McMahon, Katherine, McSweeney, Chris S., Medina, Mónica, Meredith, Laura, Mizzi, Jessica, Mock, Thomas, Momper, Lily, Moran, Mary Ann, Morgan-Lang, Connor, Moser, Duane, Muyzer, Gerard, Myrold, David, Nash, Maisie, Nesbø, Camilla L., Neumann, Anthony P., Neumann, Rebecca B., Noguera, Daniel, Northen, Trent, Norton, Jeanette, Nowinski, Brent, Nüsslein, Klaus, O’Malley, Michelle A., Oliveira, Rafael S., Maia de Oliveira, Valeria, Onstott, Tullis, Osvatic, Jay, Ouyang, Yang, Pachiadaki, Maria, Parnell, Jacob, Partida-Martinez, Laila P., Peay, Kabir G., Pelletier, Dale, Peng, Xuefeng, Pester, Michael, Pett-Ridge, Jennifer, Peura, Sari, Pjevac, Petra, Plominsky, Alvaro M., Poehlein, Anja, Pope, Phillip B., Ravin, Nikolai, Redmond, Molly C., Reiss, Rebecca, Rich, Virginia, Rinke, Christian, Rodrigues, Jorge L.Mazza, Rodriguez-Reillo, William, Rossmassler, Karen, Sackett, Joshua, Salekdeh, Ghasem Hosseini, Saleska, Scott, Scarborough, Matthew, Schachtman, Daniel, Schadt, Christopher W., Schrenk, Matthew, Sczyrba, Alexander, Sengupta, Aditi, Setubal, Joao C., Shade, Ashley, Sharp, Christine, Sherman, David H., Shubenkova, Olga V., Sierra-Garcia, Isabel Natalia, Simister, Rachel, Simon, Holly, Sjöling, Sara, Slonczewski, Joan, Correa de Souza, Rafael Soares, Spear, John R., Stegen, James C., Stepanauskas, Ramunas, Stewart, Frank, Suen, Garret, Sullivan, Matthew, Sumner, Dawn, Swan, Brandon K., Swingley, Wesley, Tarn, Jonathan, Taylor, Gordon T., Teeling, Hanno, Tekere, Memory, Teske, Andreas, Thomas, Torsten, Thrash, Cameron, Tiedje, James, Ting, Claire S., Tully, Benjamin, Ulloa, Osvlado, Valentine, David L., Van Goethem, Marc W., VanderGheynst, Jean, Verbeke, Tobin J., Vollmers, John, Vuillemin, Aurèle, Waldo, Nicholas B., Williams, Timothy J., Tyson, Gene, Woodcroft, Ben, IMG/M Data Consortium, Nayfach, Stephen, Roux, Simon, Seshadri, Rekha, Udwary, Daniel, Varghese, Neha, Schulz, Frederik, Wu, Dongying, Paez-Espino, David, Chen, I. Min, Huntemann, Marcel, Palaniappan, Krishna, Ladau, Joshua, Mukherjee, Supratim, Reddy, T. B.K., Nielsen, Torben, Kirton, Edward, Faria, José P., Edirisinghe, Janaka N., Henry, Christopher S., Jungbluth, Sean P., Chivian, Dylan, Dehal, Paramvir, Wood-Charlson, Elisha M., Arkin, Adam P., Tringe, Susannah G., Visel, Axel, Abreu, Helena, Acinas, Silvia G., Allen, Eric, Allen, Michelle A., Alteio, Lauren V., Andersen, Gary, Anesio, Alexandre M., Attwood, Graeme, Avila-Magaña, Viridiana, Badis, Yacine, Bailey, Jake, Baker, Brett, Baldrian, Petr, Barton, Hazel A., Beck, David A.C., Becraft, Eric D., Beller, Harry R., Beman, J. Michael, Bernier-Latmani, Rizlan, Berry, Timothy D., Bertagnolli, Anthony, Bertilsson, Stefan, Bhatnagar, Jennifer M., Bird, Jordan T., Blanchard, Jeffrey L., Blumer-Schuette, Sara E., Bohannan, Brendan, Borton, Mikayla A., Brady, Allyson, Brawley, Susan H., Brodie, Juliet, Brown, Steven, Brum, Jennifer R., Brune, Andreas, Bryant, Donald A., Buchan, Alison, Buckley, Daniel H., Buongiorno, Joy, Cadillo-Quiroz, Hinsby, Caffrey, Sean M., Campbell, Ashley N., Campbell, Barbara, Carr, Stephanie, Carroll, Jo Lynn, Cary, S. Craig, Cates, Anna M., Cattolico, Rose Ann, Cavicchioli, Ricardo, Chistoserdova, Ludmila, Coleman, Maureen L., Constant, Philippe, Conway, Jonathan M., Mac Cormack, Walter P., Crowe, Sean, Crump, Byron, Currie, Cameron, Daly, Rebecca, DeAngelis, Kristen M., Denef, Vincent, Denman, Stuart E., Desta, Adey, Dionisi, Hebe, Dodsworth, Jeremy, Dombrowski, Nina, Donohue, Timothy, Dopson, Mark, Driscoll, Timothy, Dunfield, Peter, Dupont, Christopher L., Dynarski, Katherine A., Edgcomb, Virginia, Edwards, Elizabeth A., Elshahed, Mostafa S., Figueroa, Israel, Flood, Beverly, Fortney, Nathaniel, Fortunato, Caroline S., Francis, Christopher, Gachon, Claire M.M., Garcia, Sarahi L., Gazitua, Maria C., Gentry, Terry, Gerwick, Lena, Gharechahi, Javad, Girguis, Peter, Gladden, John, Gradoville, Mary, Grasby, Stephen E., Gravuer, Kelly, Grettenberger, Christen L., Gruninger, Robert J., Guo, Jiarong, Habteselassie, Mussie Y., Hallam, Steven J., Hatzenpichler, Roland, Hausmann, Bela, Hazen, Terry C., Hedlund, Brian, Henny, Cynthia, Herfort, Lydie, Hernandez, Maria, Hershey, Olivia S., Hess, Matthias, Hollister, Emily B., Hug, Laura A., Hunt, Dana, Jansson, Janet, Jarett, Jessica, Kadnikov, Vitaly V., Kelly, Charlene, Kelly, Robert, Kelly, William, Kerfeld, Cheryl A., Kimbrel, Jeff, Klassen, Jonathan L., Konstantinidis, Konstantinos T., Lee, Laura L., Li, Wen Jun, Loder, Andrew J., Loy, Alexander, Lozada, Mariana, MacGregor, Barbara, Magnabosco, Cara, Maria da Silva, Aline, McKay, R. Michael, McMahon, Katherine, McSweeney, Chris S., Medina, Mónica, Meredith, Laura, Mizzi, Jessica, Mock, Thomas, Momper, Lily, Moran, Mary Ann, Morgan-Lang, Connor, Moser, Duane, Muyzer, Gerard, Myrold, David, Nash, Maisie, Nesbø, Camilla L., Neumann, Anthony P., Neumann, Rebecca B., Noguera, Daniel, Northen, Trent, Norton, Jeanette, Nowinski, Brent, Nüsslein, Klaus, O’Malley, Michelle A., Oliveira, Rafael S., Maia de Oliveira, Valeria, Onstott, Tullis, Osvatic, Jay, Ouyang, Yang, Pachiadaki, Maria, Parnell, Jacob, Partida-Martinez, Laila P., Peay, Kabir G., Pelletier, Dale, Peng, Xuefeng, Pester, Michael, Pett-Ridge, Jennifer, Peura, Sari, Pjevac, Petra, Plominsky, Alvaro M., Poehlein, Anja, Pope, Phillip B., Ravin, Nikolai, Redmond, Molly C., Reiss, Rebecca, Rich, Virginia, Rinke, Christian, Rodrigues, Jorge L.Mazza, Rodriguez-Reillo, William, Rossmassler, Karen, Sackett, Joshua, Salekdeh, Ghasem Hosseini, Saleska, Scott, Scarborough, Matthew, Schachtman, Daniel, Schadt, Christopher W., Schrenk, Matthew, Sczyrba, Alexander, Sengupta, Aditi, Setubal, Joao C., Shade, Ashley, Sharp, Christine, Sherman, David H., Shubenkova, Olga V., Sierra-Garcia, Isabel Natalia, Simister, Rachel, Simon, Holly, Sjöling, Sara, Slonczewski, Joan, Correa de Souza, Rafael Soares, Spear, John R., Stegen, James C., Stepanauskas, Ramunas, Stewart, Frank, Suen, Garret, Sullivan, Matthew, Sumner, Dawn, Swan, Brandon K., Swingley, Wesley, Tarn, Jonathan, Taylor, Gordon T., Teeling, Hanno, Tekere, Memory, Teske, Andreas, Thomas, Torsten, Thrash, Cameron, Tiedje, James, Ting, Claire S., Tully, Benjamin, Ulloa, Osvlado, Valentine, David L., Van Goethem, Marc W., VanderGheynst, Jean, Verbeke, Tobin J., Vollmers, John, Vuillemin, Aurèle, Waldo, Nicholas B., Williams, Timothy J., Tyson, Gene, Woodcroft, Ben, and IMG/M Data Consortium

Abstract

The reconstruction of bacterial and archaeal genomes from shotgun metagenomes has enabled insights into the ecology and evolution of environmental and host-associated microbiomes. Here we applied this approach to >10,000 metagenomes collected from diverse habitats covering all of Earth’s continents and oceans, including metagenomes from human and animal hosts, engineered environments, and natural and agricultural soils, to capture extant microbial, metabolic and functional potential. This comprehensive catalog includes 52,515 metagenome-assembled genomes representing 12,556 novel candidate species-level operational taxonomic units spanning 135 phyla. The catalog expands the known phylogenetic diversity of bacteria and archaea by 44% and is broadly available for streamlined comparative analyses, interactive exploration, metabolic modeling and bulk download. We demonstrate the utility of this collection for understanding secondary-metabolite biosynthetic potential and for resolving thousands of new host linkages to uncultivated viruses. This resource underscores the value of genome-centric approaches for revealing genomic properties of uncultivated microorganisms that affect ecosystem processes.

Published
2021

16. Synthase-Selective Exploration of a Tunicate Microbiome by Activity-Guided Single-Cell Genomics

Author

Kim, Woojoo E., Charov, Katherine, Džunková, Mária, Becraft, Eric D., Brown, Julia, Schulz, Frederik, Woyke, Tanja, La Clair, James J., Stepanauskas, Ramunas, Burkart, Michael D., Kim, Woojoo E., Charov, Katherine, Džunková, Mária, Becraft, Eric D., Brown, Julia, Schulz, Frederik, Woyke, Tanja, La Clair, James J., Stepanauskas, Ramunas, and Burkart, Michael D.

Abstract

While thousands of environmental metagenomes have been mined for the presence of novel biosynthetic gene clusters, such computational predictions do not provide evidence of their in vivo biosynthetic functionality. Using fluorescent in situ enzyme assay targeting carrier proteins common to polyketide (PKS) and nonribosomal peptide synthetases (NRPS), we applied fluorescence-activated cell sorting to tunicate microbiome to enrich for microbes with active secondary metabolic capabilities. Single-cell genomics uncovered the genetic basis for a wide biosynthetic diversity in the enzyme-active cells and revealed a member of marine Oceanospirillales harboring a novel NRPS gene cluster with high similarity to phylogenetically distant marine and terrestrial bacteria. Interestingly, this synthase belongs to a larger class of siderophore biosynthetic gene clusters commonly associated with pestilence and disease. This demonstrates activity-guided single-cell genomics as a tool to guide novel biosynthetic discovery.

Published
2021
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18. Ancestral Absence of Electron Transport Chains in Patescibacteria and DPANN

Author

Beam, Jacob P., primary, Becraft, Eric D., additional, Brown, Julia M., additional, Schulz, Frederik, additional, Jarett, Jessica K., additional, Bezuidt, Oliver, additional, Poulton, Nicole J., additional, Clark, Kayla, additional, Dunfield, Peter F., additional, Ravin, Nikolai V., additional, Spear, John R., additional, Hedlund, Brian P., additional, Kormas, Konstantinos A., additional, Sievert, Stefan M., additional, Elshahed, Mostafa S., additional, Barton, Hazel A., additional, Stott, Matthew B., additional, Eisen, Jonathan A., additional, Moser, Duane P., additional, Onstott, Tullis C., additional, Woyke, Tanja, additional, and Stepanauskas, Ramunas, additional

Published
2020
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19. Hiding in Plain Sight: The Globally Distributed Bacterial Candidate Phylum PAUC34f

Author

Chen, Michael L., primary, Becraft, Eric D., additional, Pachiadaki, Maria, additional, Brown, Julia M., additional, Jarett, Jessica K., additional, Gasol, Josep M., additional, Ravin, Nikolai V., additional, Moser, Duane P., additional, Nunoura, Takuro, additional, Herndl, Gerhard J., additional, Woyke, Tanja, additional, and Stepanauskas, Ramunas, additional

Published
2020
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22. Hiding in plain sight: The globally distributed bacterial candidate phylum PAUC34f

Author

Chen, Michael L., Becraft, Eric D., Pachiadaki, Maria, Brown, Julia M., Jarett, Jessica K., Gasol, Josep M., Ravin, Nikolai V., Moser, Duane P., Nunoura, Takuro, Herndl, Gerhard J., Woyke, Tanja, Stepanauskas, Ramunas, Chen, Michael L., Becraft, Eric D., Pachiadaki, Maria, Brown, Julia M., Jarett, Jessica K., Gasol, Josep M., Ravin, Nikolai V., Moser, Duane P., Nunoura, Takuro, Herndl, Gerhard J., Woyke, Tanja, and Stepanauskas, Ramunas

Abstract

Bacterial candidate phylum PAUC34f was originally discovered in marine sponges and is widely considered to be composed of sponge symbionts. Here, we report 21 single amplified genomes (SAGs) of PAUC34f from a variety of environments, including the dark ocean, lake sediments, and a terrestrial aquifer. The diverse origins of the SAGs and the results of metagenome fragment recruitment suggest that some PAUC34f lineages represent relatively abundant, free-living cells in environments other than sponge microbiomes, including the deep ocean. Both phylogenetic and biogeographic patterns, as well as genome content analyses suggest that PAUC34f associations with hosts evolved independently multiple times, while free-living lineages of PAUC34f are distinct and relatively abundant in a wide range of environments. © Copyright © 2020 Chen, Becraft, Pachiadaki, Brown, Jarett, Gasol, Ravin, Moser, Nunoura, Herndl, Woyke and Stepanauskas.

Published
2020

23. Ancestral absence of electron transport chains in Patescibacteria and DPANN

Author

Beam, Jacob P., Becraft, Eric D., Brown, Julia M., Schulz, Frederik, Jarett, Jessica K., Bezuidt, Oliver, Poulton, Nicole J., Clark, Kayla, Dunfield, Peter F., Ravin, Nikolai V., Spear, John R., Hedlund, Brian P., Kormas, Konstantinos Ar., Sievert, Stefan M., Elshahed, Mostafa S., Barton, Hazel A., Stott, Matthew B., Eisen, Jonathan A., Moser, Duane P., Onstott, Tullis C., Woyke, Tanja, Stepanauskas, Ramunas, Beam, Jacob P., Becraft, Eric D., Brown, Julia M., Schulz, Frederik, Jarett, Jessica K., Bezuidt, Oliver, Poulton, Nicole J., Clark, Kayla, Dunfield, Peter F., Ravin, Nikolai V., Spear, John R., Hedlund, Brian P., Kormas, Konstantinos Ar., Sievert, Stefan M., Elshahed, Mostafa S., Barton, Hazel A., Stott, Matthew B., Eisen, Jonathan A., Moser, Duane P., Onstott, Tullis C., Woyke, Tanja, and Stepanauskas, Ramunas

Abstract

© The Author(s), 2020. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Beam, J. P., Becraft, E. D., Brown, J. M., Schulz, F., Jarett, J. K., Bezuidt, O., Poulton, N. J., Clark, K., Dunfield, P. F., Ravin, N. V., Spear, J. R., Hedlund, B. P., Kormas, K. A., Sievert, S. M., Elshahed, M. S., Barton, H. A., Stott, M. B., Eisen, J. A., Moser, D. P., Onstott, T. C., Woyke, T., & Stepanauskas, R. Ancestral absence of electron transport chains in Patescibacteria and DPANN. Frontiers in Microbiology, 11, (2020): 1848, doi:10.3389/fmicb.2020.01848., Recent discoveries suggest that the candidate superphyla Patescibacteria and DPANN constitute a large fraction of the phylogenetic diversity of Bacteria and Archaea. Their small genomes and limited coding potential have been hypothesized to be ancestral adaptations to obligate symbiotic lifestyles. To test this hypothesis, we performed cell–cell association, genomic, and phylogenetic analyses on 4,829 individual cells of Bacteria and Archaea from 46 globally distributed surface and subsurface field samples. This confirmed the ubiquity and abundance of Patescibacteria and DPANN in subsurface environments, the small size of their genomes and cells, and the divergence of their gene content from other Bacteria and Archaea. Our analyses suggest that most Patescibacteria and DPANN in the studied subsurface environments do not form specific physical associations with other microorganisms. These data also suggest that their unusual genomic features and prevalent auxotrophies may be a result of ancestral, minimal cellular energy transduction mechanisms that lack respiration, thus relying solely on fermentation for energy conservation., This work was funded by the USA National Science Foundation grants 1441717, 1826734, and 1335810 (to RS); and 1460861 (REU site at Bigelow Laboratory for Ocean Sciences). RS was also supported by the Simons Foundation grant 510023. TW, FS, and JJ were funded by the U.S. Department of Energy Joint Genome Institute, a DOE Office of Science User Facility supported under Contract No. DE-AC02-05CH11231. NR group was funded by the Russian Science Foundation (grant 19-14-00245). SS was funded by USA National Science Foundation grants OCE-0452333 and OCE-1136727. BH was funded by NASA Exobiology grant 80NSSC17K0548.

Published
2020

24. Hiding in Plain Sight: The Globally Distributed Bacterial Candidate Phylum PAUC34f

Author

National Science Foundation (US), Simons Foundation, Ministry of Education and Science of the Russian Federation, Austrian Science Fund, European Commission, Ministerio de Ciencia, Innovación y Universidades (España), Department of Energy (US), Agencia Estatal de Investigación (España), Chen, Michael L., Becraft, Eric D., Pachiadaki, Maria, Brown, Julia M., Jarett, Jessica K., Gasol, Josep M., Ravin, Nikolai V., Moser, Duane P., Nunoura, Takuro, Herndl, Gerhard J., Woyke, Tanja, Stepanauskas, R., National Science Foundation (US), Simons Foundation, Ministry of Education and Science of the Russian Federation, Austrian Science Fund, European Commission, Ministerio de Ciencia, Innovación y Universidades (España), Department of Energy (US), Agencia Estatal de Investigación (España), Chen, Michael L., Becraft, Eric D., Pachiadaki, Maria, Brown, Julia M., Jarett, Jessica K., Gasol, Josep M., Ravin, Nikolai V., Moser, Duane P., Nunoura, Takuro, Herndl, Gerhard J., Woyke, Tanja, and Stepanauskas, R.

Abstract

Bacterial candidate phylum PAUC34f was originally discovered in marine sponges and is widely considered to be composed of sponge symbionts. Here, we report 21 single amplified genomes (SAGs) of PAUC34f from a variety of environments, including the dark ocean, lake sediments, and a terrestrial aquifer. The diverse origins of the SAGs and the results of metagenome fragment recruitment suggest that some PAUC34f lineages represent relatively abundant, free-living cells in environments other than sponge microbiomes, including the deep ocean. Both phylogenetic and biogeographic patterns, as well as genome content analyses suggest that PAUC34f associations with hosts evolved independently multiple times, while free-living lineages of PAUC34f are distinct and relatively abundant in a wide range of environments

Published
2020

26. Hydrogen-based metabolism – an ancestral trait in lineages sibling to the Cyanobacteria

Author

Matheus Carnevali, Paula B., primary, Schulz, Frederik, additional, Castelle, Cindy J., additional, Kantor, Rose, additional, Shih, Patrick, additional, Sharon, Itai, additional, Santini, Joanne M., additional, Olm, Matthew, additional, Amano, Yuki, additional, Thomas, Brian C., additional, Anantharaman, Karthik, additional, Burstein, David, additional, Becraft, Eric D., additional, Stepanauskas, Ramunas, additional, Woyke, Tanja, additional, and Banfield, Jillian F., additional

Published
2018
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27. Corrigendum: Minimum information about a single amplified genome (MISAG) and a metagenome-assembled genome (MIMAG) of bacteria and archaea (Nature Biotechnology (2017) 35 (725-731) DOI: 10.1038/nbt.3893)

Author

Bowers, Robert M., Kyrpides, Nikos C., Stepanauskas, Ramunas, Harmon-Smith, Miranda, Doud, Devin, Reddy, T. B.K., Schulz, Frederik, Jarett, Jessica, Rivers, Adam R., Eloe-Fadrosh, Emiley A., Tringe, Susannah G., Ivanova, Natalia N., Copeland, Alex, Clum, Alicia, Becraft, Eric D., Malmstrom, Rex R., Birren, Bruce, Podar, Mircea, Bork, Peer, Weinstock, George M., Garrity, George M., Dodsworth, Jeremy A., Yooseph, Shibu, Sutton, Granger, Glöckner, Frank O., Gilbert, Jack A., Nelson, William C., Hallam, Steven J., Jungbluth, Sean P., Ettema, Thijs J.G., Tighe, Scott, Konstantinidis, Konstantinos T., Liu, Wen Tso, Baker, Brett J., Rattei, Thomas, Eisen, Jonathan A., Hedlund, Brian, McMahon, Katherine D., Fierer, Noah, Knight, Rob, Finn, Rob, Cochrane, Guy, Karsch-Mizrachi, Ilene, Tyson, Gene W., Rinke, Christian, Lapidus, Alla, Meyer, Folker, Yilmaz, Pelin, Parks, Donovan H., Eren, A. M., Schriml, Lynn, Banfield, Jillian F., Hugenholtz, Philip, Woyke, Tanja, other, and, Bowers, Robert M., Kyrpides, Nikos C., Stepanauskas, Ramunas, Harmon-Smith, Miranda, Doud, Devin, Reddy, T. B.K., Schulz, Frederik, Jarett, Jessica, Rivers, Adam R., Eloe-Fadrosh, Emiley A., Tringe, Susannah G., Ivanova, Natalia N., Copeland, Alex, Clum, Alicia, Becraft, Eric D., Malmstrom, Rex R., Birren, Bruce, Podar, Mircea, Bork, Peer, Weinstock, George M., Garrity, George M., Dodsworth, Jeremy A., Yooseph, Shibu, Sutton, Granger, Glöckner, Frank O., Gilbert, Jack A., Nelson, William C., Hallam, Steven J., Jungbluth, Sean P., Ettema, Thijs J.G., Tighe, Scott, Konstantinidis, Konstantinos T., Liu, Wen Tso, Baker, Brett J., Rattei, Thomas, Eisen, Jonathan A., Hedlund, Brian, McMahon, Katherine D., Fierer, Noah, Knight, Rob, Finn, Rob, Cochrane, Guy, Karsch-Mizrachi, Ilene, Tyson, Gene W., Rinke, Christian, Lapidus, Alla, Meyer, Folker, Yilmaz, Pelin, Parks, Donovan H., Eren, A. M., Schriml, Lynn, Banfield, Jillian F., Hugenholtz, Philip, Woyke, Tanja, and other, and

Abstract

In the version of this article initially published, the author A. Murat Eren was listed as A.M. Eren. The corresponding affiliation was given as the Knapp Center for Biomedical Discovery, rather than Department of Medicine, University of Chicago, Chicago, Illinois, USA, and Marine Biological Laboratory, Woods Hole, Massachusetts, USA. The errors have been corrected in the HTML and PDF versions of the article as of 29 November 2017. In the version of this article initially published, the following acknowledgment was omitted: A.L. was supported by the Russian Science Foundation (grant number 14-50-00069). The error has been corrected in the HTML and PDF versions of the article as of 7 December 2017.

Published
2018

28. Correction: Corrigendum: Minimum information about a single amplified genome (MISAG) and a metagenome-assembled genome (MIMAG) of bacteria and archaea

Author

Woyke, Tanja, Hugenholtz, Philip, Banfield, Jillian F., Schriml, Lynn, Eren, A. M., Parks, Donovan H., Yilmaz, Pelin, Meyer, Folker, Lapidus, Alla, Rinke, Christian, Tyson, Gene W., Karsch-Mizrachi, Ilene, Cochrane, Guy, Finn, Rob, Knight, Rob, Fierer, Noah, McMahon, Katherine D., Hedlund, Brian, Eisen, Jonathan A., Rattei, Thomas, Baker, Brett J., Liu, Wen-Tso, Konstantinidis, Konstantinos T., Tighe, Scott, Ettema, Thijs J. G., Jungbluth, Sean P., Hallam, Steven J., Nelson, William C., Gilbert, Jack A., Glockner, Frank O., Sutton, Granger, Yooseph, Shibu, Dodsworth, Jeremy A., Garrity, George M., Weinstock, George M., Bork, Peer, Podar, Mircea, Birren, Bruce, Malmstrom, Rex R., Becraft, Eric D., Clum, Alicia, Copeland, Alex, Ivanova, Natalia N., Tringe, Susannah G., Eloe-Fadrosh, Emiley A., Rivers, Adam R., Jarett, Jessica, Schulz, Frederik, Reddy, T. B. K., Doud, Devin, Harmon-Smith, Miranda, Stepanauskas, Ramunas, Kyrpides, Nikos C., Bowers, Robert M., Woyke, Tanja, Hugenholtz, Philip, Banfield, Jillian F., Schriml, Lynn, Eren, A. M., Parks, Donovan H., Yilmaz, Pelin, Meyer, Folker, Lapidus, Alla, Rinke, Christian, Tyson, Gene W., Karsch-Mizrachi, Ilene, Cochrane, Guy, Finn, Rob, Knight, Rob, Fierer, Noah, McMahon, Katherine D., Hedlund, Brian, Eisen, Jonathan A., Rattei, Thomas, Baker, Brett J., Liu, Wen-Tso, Konstantinidis, Konstantinos T., Tighe, Scott, Ettema, Thijs J. G., Jungbluth, Sean P., Hallam, Steven J., Nelson, William C., Gilbert, Jack A., Glockner, Frank O., Sutton, Granger, Yooseph, Shibu, Dodsworth, Jeremy A., Garrity, George M., Weinstock, George M., Bork, Peer, Podar, Mircea, Birren, Bruce, Malmstrom, Rex R., Becraft, Eric D., Clum, Alicia, Copeland, Alex, Ivanova, Natalia N., Tringe, Susannah G., Eloe-Fadrosh, Emiley A., Rivers, Adam R., Jarett, Jessica, Schulz, Frederik, Reddy, T. B. K., Doud, Devin, Harmon-Smith, Miranda, Stepanauskas, Ramunas, Kyrpides, Nikos C., and Bowers, Robert M.

Abstract

Nat. Biotechnol. 35, 725–731 (2017); published online 8 August 2017; corrected after print 29 November 2017; corrected after print 7 December 2017 In the version of this article initially published, the author A. Murat Eren was listed as A.M. Eren. The corresponding affiliation was given as the Knapp Center for Biomedical Discovery, rather than Department of Medicine, University of Chicago, Chicago, Illinois, USA, and Marine Biological Laboratory, Woods Hole, Massachusetts, USA. The errors have been corrected in the HTML and PDF versions of the article as of 29 November 2017. In the version of this article initially published, the following acknowledgment was omitted: A.L. was supported by the Russian Science Foundation (grant number 14-50-00069). The error has been corrected in the HTML and PDF versions of the article as of 7 December 2017.

Published
2018

29. Erratum: Corrigendum: Minimum information about a single amplified genome (MISAG) and a metagenome-assembled genome (MIMAG) of bacteria and archaea

Author

Bowers, Robert M, Kyrpides, Nikos C, Stepanauskas, Ramunas, Harmon-Smith, Miranda, Doud, Devin, Reddy, TBK, Schulz, Frederik, Jarett, Jessica, Rivers, Adam R, Eloe-Fadrosh, Emiley A, Tringe, Susannah G, Ivanova, Natalia N, Copeland, Alex, Clum, Alicia, Becraft, Eric D, Malmstrom, Rex R, Birren, Bruce, Podar, Mircea, Bork, Peer, Weinstock, George M, Garrity, George M, Dodsworth, Jeremy A, Yooseph, Shibu, Sutton, Granger, Glöckner, Frank O, Gilbert, Jack A, Nelson, William C, Hallam, Steven J, Jungbluth, Sean P, Ettema, Thijs JG, Tighe, Scott, Konstantinidis, Konstantinos T, Liu, Wen-Tso, Baker, Brett J, Rattei, Thomas, Eisen, Jonathan A, Hedlund, Brian, McMahon, Katherine D, Fierer, Noah, Knight, Rob, Finn, Rob, Cochrane, Guy, Karsch-Mizrachi, Ilene, Tyson, Gene W, Rinke, Christian, Lapidus, Alla, Meyer, Folker, Yilmaz, Pelin, Parks, Donovan H, Eren, AM, Schriml, Lynn, Banfield, Jillian F, Hugenholtz, Philip, Woyke, Tanja, Bowers, Robert M, Kyrpides, Nikos C, Stepanauskas, Ramunas, Harmon-Smith, Miranda, Doud, Devin, Reddy, TBK, Schulz, Frederik, Jarett, Jessica, Rivers, Adam R, Eloe-Fadrosh, Emiley A, Tringe, Susannah G, Ivanova, Natalia N, Copeland, Alex, Clum, Alicia, Becraft, Eric D, Malmstrom, Rex R, Birren, Bruce, Podar, Mircea, Bork, Peer, Weinstock, George M, Garrity, George M, Dodsworth, Jeremy A, Yooseph, Shibu, Sutton, Granger, Glöckner, Frank O, Gilbert, Jack A, Nelson, William C, Hallam, Steven J, Jungbluth, Sean P, Ettema, Thijs JG, Tighe, Scott, Konstantinidis, Konstantinos T, Liu, Wen-Tso, Baker, Brett J, Rattei, Thomas, Eisen, Jonathan A, Hedlund, Brian, McMahon, Katherine D, Fierer, Noah, Knight, Rob, Finn, Rob, Cochrane, Guy, Karsch-Mizrachi, Ilene, Tyson, Gene W, Rinke, Christian, Lapidus, Alla, Meyer, Folker, Yilmaz, Pelin, Parks, Donovan H, Eren, AM, Schriml, Lynn, Banfield, Jillian F, Hugenholtz, Philip, and Woyke, Tanja

Published
2018

30. Author Correction: Improved genome recovery and integrated cell-size analyses of individual uncultured microbial cells and viral particles

Author

Stepanauskas, Ramunas, primary, Fergusson, Elizabeth A., additional, Brown, Joseph, additional, Poulton, Nicole J., additional, Tupper, Ben, additional, Labonté, Jessica M., additional, Becraft, Eric D., additional, Brown, Julia M., additional, Pachiadaki, Maria G., additional, Povilaitis, Tadas, additional, Thompson, Brian P., additional, Mascena, Corianna J., additional, Bellows, Wendy K., additional, and Lubys, Arvydas, additional

Published
2017
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32. Solagigasbacteria: Lone genomic giants among the uncultured bacterial phyla

Author

Becraft, Eric D., primary, Woyke, Tanja, additional, Jarett, Jessica, additional, Ivanova, Natalia, additional, Vitorino, Filipa Godoy, additional, Poulton, Nicole, additional, Brown, Julia M., additional, Brown, Joseph, additional, Lau, C.Y.M., additional, Onstott, Tullis, additional, Eisen, Jonathan A., additional, Moser, Duane, additional, and Stepanauskas, Ramunas, additional

Published
2017
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33. Minimum information about a single amplified genome (MISAG) and a metagenome-assembled genome (MIMAG) of bacteria and archaea

Author

Bowers, Robert M., Kyrpides, Nikos C., Stepanauskas, Ramunas, Harmon-Smith, Miranda, Doud, Devin, Reddy, T. B. K., Schulz, Frederik, Jarett, Jessica, Rivers, Adam R., Eloe-Fadrosh, Emiley A., Tringe, Susannah G., Ivanova, Natalia N., Copeland, Alex, Clum, Alicia, Becraft, Eric D., Malmstrom, Rex R., Birren, Bruce, Podar, Mircea, Bork, Peer, Weinstock, George M., Garrity, George M., Dodsworth, Jeremy A., Yooseph, Shibu, Sutton, Granger, Gloeckner, Frank O., Gilbert, Jack A., Nelson, William C., Hallam, Steven J., Jungbluth, Sean P., Ettema, Thijs J. G., Tighe, Scott, Konstantinidis, Konstantinos T., Liu, Wen-Tso, Baker, Brett J., Rattei, Thomas, Eisen, Jonathan A., Hedlund, Brian, McMahon, Katherine D., Fierer, Noah, Knight, Rob, Finn, Rob, Cochrane, Guy, Karsch-Mizrachi, Ilene, Tyson, Gene W., Rinke, Christian, Lapidus, Alla, Meyer, Folker, Yilmaz, Pelin, Parks, Donovan H., Eren, A. M., Schriml, Lynn, Banfield, Jillian F., Hugenholtz, Philip, Woyke, Tanja, Bowers, Robert M., Kyrpides, Nikos C., Stepanauskas, Ramunas, Harmon-Smith, Miranda, Doud, Devin, Reddy, T. B. K., Schulz, Frederik, Jarett, Jessica, Rivers, Adam R., Eloe-Fadrosh, Emiley A., Tringe, Susannah G., Ivanova, Natalia N., Copeland, Alex, Clum, Alicia, Becraft, Eric D., Malmstrom, Rex R., Birren, Bruce, Podar, Mircea, Bork, Peer, Weinstock, George M., Garrity, George M., Dodsworth, Jeremy A., Yooseph, Shibu, Sutton, Granger, Gloeckner, Frank O., Gilbert, Jack A., Nelson, William C., Hallam, Steven J., Jungbluth, Sean P., Ettema, Thijs J. G., Tighe, Scott, Konstantinidis, Konstantinos T., Liu, Wen-Tso, Baker, Brett J., Rattei, Thomas, Eisen, Jonathan A., Hedlund, Brian, McMahon, Katherine D., Fierer, Noah, Knight, Rob, Finn, Rob, Cochrane, Guy, Karsch-Mizrachi, Ilene, Tyson, Gene W., Rinke, Christian, Lapidus, Alla, Meyer, Folker, Yilmaz, Pelin, Parks, Donovan H., Eren, A. M., Schriml, Lynn, Banfield, Jillian F., Hugenholtz, Philip, and Woyke, Tanja

Abstract

We present two standards developed by the Genomic Standards Consortium (GSC) for reporting bacterial and archaeal genome sequences. Both are extensions of the Minimum Information about Any (x) Sequence (MIxS). The standards are the Minimum Information about a Single Amplified Genome (MISAG) and the Minimum Information about a Metagenome-Assembled Genome (MIMAG), including, but not limited to, assembly quality, and estimates of genome completeness and contamination. These standards can be used in combination with other GSC checklists, including the Minimum Information about a Genome Sequence (MIGS), Minimum Information about a Metagenomic Sequence (MIMS), and Minimum Information about a Marker Gene Sequence (MIMARKS). Community-wide adoption of MISAG and MIMAG will facilitate more robust comparative genomic analyses of bacterial and archaeal diversity.

Published
2017
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34. Single-Cell-Genomics-Facilitated Read Binning of Candidate Phylum EM19 Genomes from Geothermal Spring Metagenomes

Author

Becraft, Eric D., primary, Dodsworth, Jeremy A., additional, Murugapiran, Senthil K., additional, Ohlsson, J. Ingemar, additional, Briggs, Brandon R., additional, Kanbar, Jad, additional, De Vlaminck, Iwijn, additional, Quake, Stephen R., additional, Dong, Hailiang, additional, Hedlund, Brian P., additional, and Swingley, Wesley D., additional

Published
2016
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36. Diel metabolomics analysis of a hot spring chlorophototrophic microbial mat leads to new hypotheses of community member metabolisms

Author

Kim, Young-Mo, Nowack, Shane, Olsen, Millie T., Becraft, Eric D., Wood, Jason M., Thiel, Vera, Klapper, Isaac, Kühl, Michael, Fredrickson, James K., Bryant, Donald A., Ward, David M., Metz, Thomas O., Kim, Young-Mo, Nowack, Shane, Olsen, Millie T., Becraft, Eric D., Wood, Jason M., Thiel, Vera, Klapper, Isaac, Kühl, Michael, Fredrickson, James K., Bryant, Donald A., Ward, David M., and Metz, Thomas O.

Published
2015

37. The molecular dimension of microbial species:1. Ecological distinctions among, and homogeneity within, putative ecotypes of Synechococcus inhabiting the cyanobacterial mat of Mushroom Spring, Yellowstone National Park

Author

Becraft, Eric D., Wood, Jason M., Rusch, Douglas B., Kühl, Michael, Jensen, Sheila Ingemann, Bryant, Donald A., Roberts, David W., Cohan, Frederick M., Ward, David M., Becraft, Eric D., Wood, Jason M., Rusch, Douglas B., Kühl, Michael, Jensen, Sheila Ingemann, Bryant, Donald A., Roberts, David W., Cohan, Frederick M., and Ward, David M.

Published
2015

38. The molecular dimension of microbial species: 1. Ecological distinctions among, and homogeneity within, putative ecotypes of Synechococcus inhabiting the cyanobacterial mat of Mushroom Spring, Yellowstone National Park

Author

Becraft, Eric D., Wood, Jason M., Rusch, Douglas B., Kühl, Michael, Ingemann Jensen, Sheila, Bryant, Donald A., Roberts, David W., Cohan, Frederick M., Ward, David M., Becraft, Eric D., Wood, Jason M., Rusch, Douglas B., Kühl, Michael, Ingemann Jensen, Sheila, Bryant, Donald A., Roberts, David W., Cohan, Frederick M., and Ward, David M.

Abstract

Based on the Stable Ecotype Model, evolution leads to the divergence of ecologically distinct populations (e.g., with different niches and/or behaviors) of ecologically interchangeable membership. In this study, pyrosequencing was used to provide deep sequence coverage of Synechococcus psaA genes and transcripts over a large number of habitat types in the Mushroom Spring microbial mat. Putative ecological species [putative ecotypes (PEs)], which were predicted by an evolutionary simulation based on the Stable Ecotype Model (Ecotype Simulation), exhibited distinct distributions relative to temperature-defined positions in the effluent channel and vertical position in the upper 1 mm-thick mat layer. Importantly, in most cases variants predicted to belong to the same PE formed unique clusters relative to temperature and depth in the mat in canonical correspondence analysis, supporting the hypothesis that while the PEs are ecologically distinct, the members of each ecotype are ecologically homogeneous. PEs responded differently to experimental perturbations of temperature and light, but the genetic variation within each PE was maintained as the relative abundances of PEs changed, further indicating that each population responded as a set of ecologically interchangeable individuals. Compared to PEs that predominate deeper within the mat photic zone, the timing of transcript abundances for selected genes differed for PEs that predominate in microenvironments closer to upper surface of the mat with spatiotemporal differences in light and O2 concentration. All of these findings are consistent with the hypotheses that Synechococcus species in hot spring mats are sets of ecologically interchangeable individuals that are differently adapted, that these adaptations control their distributions, and that the resulting distributions constrain the activities of the species in space and time.

Published
2015

39. The molecular dimension of microbial species: 2. Synechococcus strains representative of putative ecotypes inhabiting different depths in the Mushroom Spring microbial mat exhibit different adaptive and acclimative responses to light

Author

Nowack, Shane, primary, Olsen, Millie T., additional, Schaible, George A., additional, Becraft, Eric D., additional, Shen, Gaozhong, additional, Klapper, Isaac, additional, Bryant, Donald A., additional, and Ward, David M., additional

Published
2015
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40. The molecular dimension of microbial species: 3. Comparative genomics of Synechococcus strains with different light responses and in situ diel transcription patterns of associated putative ecotypes in the Mushroom Spring microbial mat

Author

Olsen, Millie T., primary, Nowack, Shane, additional, Wood, Jason M., additional, Becraft, Eric D., additional, LaButti, Kurt, additional, Lipzen, Anna, additional, Martin, Joel, additional, Schackwitz, Wendy S., additional, Rusch, Douglas B., additional, Cohan, Frederick M., additional, Bryant, Donald A., additional, and Ward, David M., additional

Published
2015
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41. The molecular dimension of microbial species: 1. Ecological distinctions among, and homogeneity within, putative ecotypes of Synechococcus inhabiting the cyanobacterial mat of Mushroom Spring, Yellowstone National Park

Author

Becraft, Eric D., primary, Wood, Jason M., additional, Rusch, Douglas B., additional, Kühl, Michael, additional, Jensen, Sheila I., additional, Bryant, Donald A., additional, Roberts, David W., additional, Cohan, Frederick M., additional, and Ward, David M., additional

Published
2015
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42. Diel metabolomics analysis of a hot spring chlorophototrophic microbial mat leads to new hypotheses of community member metabolisms

Author

Kim, Young-Mo, primary, Nowack, Shane, additional, Olsen, Millie T., additional, Becraft, Eric D., additional, Wood, Jason M., additional, Thiel, Vera, additional, Klapper, Isaac, additional, Kühl, Michael, additional, Fredrickson, James K., additional, Bryant, Donald A., additional, Ward, David M., additional, and Metz, Thomas O., additional

Published
2015
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43. Regulation of nif gene expression and the energetics of N2 fixation over the diel cycle in a hot spring microbial mat.

Author

Steunou, Anne-Soisig, Jensen, Sheila I, Brecht, Eric, Becraft, Eric D, Bateson, Mary M, Kilian, Oliver, Bhaya, Devaki, Ward, David M, Peters, John W, Grossman, Arthur R, Kühl, Michael, Steunou, Anne-Soisig, Jensen, Sheila I, Brecht, Eric, Becraft, Eric D, Bateson, Mary M, Kilian, Oliver, Bhaya, Devaki, Ward, David M, Peters, John W, Grossman, Arthur R, and Kühl, Michael

Abstract

Nitrogen fixation, a prokaryotic, O(2)-inhibited process that reduces N(2) gas to biomass, is of paramount importance in biogeochemical cycling of nitrogen. We analyzed the levels of nif transcripts of Synechococcus ecotypes, NifH subunit and nitrogenase activity over the diel cycle in the microbial mat of an alkaline hot spring in Yellowstone National Park. The results showed a rise in nif transcripts in the evening, with a subsequent decline over the course of the night. In contrast, immunological data demonstrated that the level of the NifH polypeptide remained stable during the night, and only declined when the mat became oxic in the morning. Nitrogenase activity was low throughout the night; however, it exhibited two peaks, a small one in the evening and a large one in the early morning, when light began to stimulate cyanobacterial photosynthetic activity, but O(2) consumption by respiration still exceeded the rate of O(2) evolution. Once the irradiance increased to the point at which the mat became oxic, the nitrogenase activity was strongly inhibited. Transcripts for proteins associated with energy-producing metabolisms in the cell also followed diel patterns, with fermentation-related transcripts accumulating at night, photosynthesis- and respiration-related transcripts accumulating during the day and late afternoon, respectively. These results are discussed with respect to the energetics and regulation of N(2) fixation in hot spring mats and factors that can markedly influence the extent of N(2) fixation over the diel cycle.The ISME Journal (2008) 2, 364-378; doi:10.1038/ismej.2007.117; published online 6 March 2008. Udgivelsesdato: 2008-Apr

Published
2008

47. Diel metabolomics analysis of a hot spring chlorophototrophic microbial mat leads to new hypotheses of community member metabolisms.

Author

Young-Mo Kim, Nowack, Shane, Olsen, Millie T., Becraft, Eric D., Wood, Jason M., Thiel, Vera, Klapper, Isaac, Kühl, Michael, Fredrickson, James K., Bryant, Donald A., Ward, David M., and Metz, Thomas O.

Subjects
METABOLOMICS, MICROBIAL mats, METABOLITES, CLIMATE change, ORGANIC acids, WAX esters, POLYHYDROXYALKANOATES, CIRCADIAN rhythms
Abstract

Dynamic environmental factors such as light, nutrients, salt, and temperature continuously affect chlorophototrophic microbial mats, requiring adaptive and acclimative responses to stabilize composition and function. Quantitative metabolomics analysis can provide insights into metabolite dynamics for understanding community response to such changing environmental conditions. In this study, we quantified volatile organic acids, polar metabolites (amino acids, glycolytic and citric acid cycle intermediates, nucleobases, nucleosides, and sugars), wax esters, and polyhydroxyalkanoates, resulting in the identification of 104 metabolites and related molecules in thermal chlorophototrophic microbial mat cores collected over a diel cycle in Mushroom Spring, Yellowstone National Park. A limited number of predominant taxa inhabit this community and their functional potentials have been previously identified through metagenomic and metatranscriptomic analyses and in situ metabolisms, and metabolic interactions among these taxa have been hypothesized. Our metabolomics results confirmed the diel cycling of photorespiration (e.g., glycolate) and fermentation (e.g., acetate, propionate, and lactate) products, the carbon storage polymers polyhydroxyalkanoates, and dissolved gasses (e.g., H2 and CO2) in the waters overlying the mat, which were hypothesized to occur in major mat chlorophototrophic community members. In addition, we have formulated the following new hypotheses: (1) the morning hours are a time of biosynthesis of amino acids, DNA, and RNA; (2) photo-inhibited cells may also produce lactate via fermentation as an alternate metabolism; (3) glycolate and lactate are exchanged among Synechococcus and Roseiflexus spp.; and (4) fluctuations in many metabolite pools (e.g., wax esters) at different times of day result from species found at different depths within the mat responding to temporal differences in their niches. [ABSTRACT FROM AUTHOR]

Published
2015
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48. Regulation of nif gene expression and the energetics of N2 fixation over the diel cycle in a hot spring microbial mat.

Author

Steunou, Anne-Soisig, Jensen, Sheila I., Brecht, Eric, Becraft, Eric D., Bateson, Mary M., Kilian, Oliver, Bhaya, Devaki, Ward, David M., Peters, John W., Grossman, Arthur R., and Kühl, Michael

Subjects
NITROGEN fixation, PROKARYOTES, BIOMASS, BIOGEOCHEMISTRY, NITROGEN, PROTEINS
Abstract

Nitrogen fixation, a prokaryotic, O2-inhibited process that reduces N2 gas to biomass, is of paramount importance in biogeochemical cycling of nitrogen. We analyzed the levels of nif transcripts of Synechococcus ecotypes, NifH subunit and nitrogenase activity over the diel cycle in the microbial mat of an alkaline hot spring in Yellowstone National Park. The results showed a rise in nif transcripts in the evening, with a subsequent decline over the course of the night. In contrast, immunological data demonstrated that the level of the NifH polypeptide remained stable during the night, and only declined when the mat became oxic in the morning. Nitrogenase activity was low throughout the night; however, it exhibited two peaks, a small one in the evening and a large one in the early morning, when light began to stimulate cyanobacterial photosynthetic activity, but O2 consumption by respiration still exceeded the rate of O2 evolution. Once the irradiance increased to the point at which the mat became oxic, the nitrogenase activity was strongly inhibited. Transcripts for proteins associated with energy-producing metabolisms in the cell also followed diel patterns, with fermentation-related transcripts accumulating at night, photosynthesis- and respiration-related transcripts accumulating during the day and late afternoon, respectively. These results are discussed with respect to the energetics and regulation of N2 fixation in hot spring mats and factors that can markedly influence the extent of N2 fixation over the diel cycle.The ISME Journal (2008) 2, 364–378; doi:10.1038/ismej.2007.117; published online 6 March 2008 [ABSTRACT FROM AUTHOR]

Published
2008
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49. Hiding in plain sight: The globally distributed bacterial candidate phylum PAUC34f

Author

<p>Austrian Science Fund, FWF: P28781-B21</p> <p>U.S. Department of Energy, USDOE 1460861, 1232982, 1441717, 1335810</p> <p>Office of Science, SC: DE-AC02-05CH11231</p> <p>Simons Foundation, SF: 510023</p> <p>European Research Council, ERC: RTI2018-101025-B-I00, 268595</p>, Chen, Michael L., Becraft, Eric D., Pachiadaki, Maria, Brown, Julia M., Jarett, Jessica K., Gasol, Josep M., Ravin, Nikolai V., Moser, Duane P., Nunoura, Takuro, Herndl, Gerhard J., Woyke, Tanja, Stepanauskas, Ramunas, <p>Austrian Science Fund, FWF: P28781-B21</p> <p>U.S. Department of Energy, USDOE 1460861, 1232982, 1441717, 1335810</p> <p>Office of Science, SC: DE-AC02-05CH11231</p> <p>Simons Foundation, SF: 510023</p> <p>European Research Council, ERC: RTI2018-101025-B-I00, 268595</p>, Chen, Michael L., Becraft, Eric D., Pachiadaki, Maria, Brown, Julia M., Jarett, Jessica K., Gasol, Josep M., Ravin, Nikolai V., Moser, Duane P., Nunoura, Takuro, Herndl, Gerhard J., Woyke, Tanja, and Stepanauskas, Ramunas

Abstract

Chen, M. L., Becraft, E. D., Pachiadaki, M., Brown, J. M., Jarett, J. K., Gasol, J. M., ... & Woyke, T. (2020). Hiding in plain sight: The globally distributed bacterial candidate phylum PAUC34f. Frontiers in Microbiology, 11, Article 376. https://doi.org/10.3389/fmicb.2020.00376

50. Single-Cell-Genomics-Facilitated Read Binning of Candidate Phylum EM19 Genomes from Geothermal Spring Metagenomes.

Author

Becraft ED, Dodsworth JA, Murugapiran SK, Ohlsson JI, Briggs BR, Kanbar J, De Vlaminck I, Quake SR, Dong H, Hedlund BP, and Swingley WD

Subjects
China, Machine Learning, United States, Computational Biology methods, Genome, Microbial, Genomics methods, High-Throughput Nucleotide Sequencing methods, Hot Springs microbiology, Metagenomics methods
Abstract

The vast majority of microbial life remains uncatalogued due to the inability to cultivate these organisms in the laboratory. This "microbial dark matter" represents a substantial portion of the tree of life and of the populations that contribute to chemical cycling in many ecosystems. In this work, we leveraged an existing single-cell genomic data set representing the candidate bacterial phylum "Calescamantes" (EM19) to calibrate machine learning algorithms and define metagenomic bins directly from pyrosequencing reads derived from Great Boiling Spring in the U.S. Great Basin. Compared to other assembly-based methods, taxonomic binning with a read-based machine learning approach yielded final assemblies with the highest predicted genome completeness of any method tested. Read-first binning subsequently was used to extract Calescamantes bins from all metagenomes with abundant Calescamantes populations, including metagenomes from Octopus Spring and Bison Pool in Yellowstone National Park and Gongxiaoshe Spring in Yunnan Province, China. Metabolic reconstruction suggests that Calescamantes are heterotrophic, facultative anaerobes, which can utilize oxidized nitrogen sources as terminal electron acceptors for respiration in the absence of oxygen and use proteins as their primary carbon source. Despite their phylogenetic divergence, the geographically separate Calescamantes populations were highly similar in their predicted metabolic capabilities and core gene content, respiring O2, or oxidized nitrogen species for energy conservation in distant but chemically similar hot springs., (Copyright © 2016, American Society for Microbiology. All Rights Reserved.)

Published
2015
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