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1. Multicellular magnetotactic bacteria are genetically heterogeneous consortia with metabolically differentiated cells

Author

Schaible, George A, Jay, Zackary J, Cliff, John, Schulz, Frederik, Gauvin, Colin, Goudeau, Danielle, Malmstrom, Rex R, Ruff, S Emil, Edgcomb, Virginia, and Hatzenpichler, Roland

Subjects
Microbiology, Biological Sciences, Ecology, Genetics, Human Genome, Biotechnology, Generic health relevance, In Situ Hybridization, Fluorescence, Metagenome, Microbial Consortia, Genome, Bacterial, Bacteria, Genetic Variation, Phylogeny, Agricultural and Veterinary Sciences, Medical and Health Sciences, Developmental Biology, Agricultural, veterinary and food sciences, Biological sciences, Biomedical and clinical sciences
Abstract

Consortia of multicellular magnetotactic bacteria (MMB) are currently the only known example of bacteria without a unicellular stage in their life cycle. Because of their recalcitrance to cultivation, most previous studies of MMB have been limited to microscopic observations. To study the biology of these unique organisms in more detail, we use multiple culture-independent approaches to analyze the genomics and physiology of MMB consortia at single-cell resolution. We separately sequenced the metagenomes of 22 individual MMB consortia, representing 8 new species, and quantified the genetic diversity within each MMB consortium. This revealed that, counter to conventional views, cells within MMB consortia are not clonal. Single consortia metagenomes were then used to reconstruct the species-specific metabolic potential and infer the physiological capabilities of MMB. To validate genomic predictions, we performed stable isotope probing (SIP) experiments and interrogated MMB consortia using fluorescence in situ hybridization (FISH) combined with nanoscale secondary ion mass spectrometry (NanoSIMS). By coupling FISH with bioorthogonal noncanonical amino acid tagging (BONCAT), we explored their in situ activity as well as variation of protein synthesis within cells. We demonstrate that MMB consortia are mixotrophic sulfate reducers and that they exhibit metabolic differentiation between individual cells, suggesting that MMB consortia are more complex than previously thought. These findings expand our understanding of MMB diversity, ecology, genomics, and physiology, as well as offer insights into the mechanisms underpinning the multicellular nature of their unique lifestyle.

Published
2024

4. MicrobioRaman: an open-access web repository for microbiological Raman spectroscopy data

Author

Lee, Kang Soo, Landry, Zachary, Athar, Awais, Alcolombri, Uria, Pramoj Na Ayutthaya, Pratchaya, Berry, David, de Bettignies, Philippe, Cheng, Ji-Xin, Csucs, Gabor, Cui, Li, Deckert, Volker, Dieing, Thomas, Dionne, Jennifer, Doskocil, Ondrej, D’Souza, Glen, García-Timermans, Cristina, Gierlinger, Notburga, Goda, Keisuke, Hatzenpichler, Roland, Henshaw, Richard J., Huang, Wei E., Iermak, Ievgeniia, Ivleva, Natalia P., Kneipp, Janina, Kubryk, Patrick, Küsel, Kirsten, Lee, Tae Kwon, Lee, Sung Sik, Ma, Bo, Martínez-Pérez, Clara, Matousek, Pavel, Meckenstock, Rainer U., Min, Wei, Mojzeš, Peter, Müller, Oliver, Kumar, Naresh, Nielsen, Per Halkjær, Notingher, Ioan, Palatinszky, Márton, Pereira, Fátima C., Pezzotti, Giuseppe, Pilat, Zdenek, Plesinger, Filip, Popp, Jürgen, Probst, Alexander J., Riva, Alessandra, Saleh, Amr. A. E., Samek, Ota, Sapers, Haley M., Schubert, Olga T., Stubbusch, Astrid K. M., Tadesse, Loza F., Taylor, Gordon T., Wagner, Michael, Wang, Jing, Yin, Huabing, Yue, Yang, Zenobi, Renato, Zini, Jacopo, Sarkans, Ugis, and Stocker, Roman

Published
2024
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5. Community Report from the Biosignatures Standards of Evidence Workshop

Author

Meadows, Victoria, Graham, Heather, Abrahamsson, Victor, Adam, Zach, Amador-French, Elena, Arney, Giada, Barge, Laurie, Barlow, Erica, Berea, Anamaria, Bose, Maitrayee, Bower, Dina, Chan, Marjorie, Cleaves, Jim, Corpolongo, Andrea, Currie, Miles, Domagal-Goldman, Shawn, Dong, Chuanfei, Eigenbrode, Jennifer, Enright, Allison, Fauchez, Thomas J., Fisk, Martin, Fricke, Matthew, Fujii, Yuka, Gangidine, Andrew, Gezer, Eftal, Glavin, Daniel, Grenfell, Lee, Harman, Sonny, Hatzenpichler, Roland, Hausrath, Libby, Henderson, Bryana, Johnson, Sarah Stewart, Jones, Andrea, Hamilton, Trinity, Hickman-Lewis, Keyron, Jahnke, Linda, Kacar, Betul, Kopparapu, Ravi, Kempes, Christopher, Kish, Adrienne, Krissansen-Totton, Joshua, Leavitt, Wil, Komatsu, Yu, Lichtenberg, Tim, Lindsay, Melody, Maggiori, Catherine, Marais, David Des, Mathis, Cole, Morono, Yuki, Neveu, Marc, Ni, Grace, Nixon, Conor, Olson, Stephanie, Parenteau, Niki, Perl, Scott, Quinn, Richard, Raj, Chinmayee, Rodriguez, Laura, Rutter, Lindsay, Sandora, McCullen, Schmidt, Britney, Schwieterman, Eddie, Segura, Antigona, Sekerci, Fatih, Seyler, Lauren, Smith, Harrison, Soares, Georgia, Som, Sanjoy, Suzuki, Shino, Teece, Bonnie, Weber, Jessica, Wolfe-Simon, Felisa, Wong, Michael, Yano, Hajime, and Young, Liza

Subjects
Astrophysics - Instrumentation and Methods for Astrophysics, Astrophysics - Earth and Planetary Astrophysics, Quantitative Biology - Populations and Evolution
Abstract

The search for life beyond the Earth is the overarching goal of the NASA Astrobiology Program, and it underpins the science of missions that explore the environments of Solar System planets and exoplanets. However, the detection of extraterrestrial life, in our Solar System and beyond, is sufficiently challenging that it is likely that multiple measurements and approaches, spanning disciplines and missions, will be needed to make a convincing claim. Life detection will therefore not be an instantaneous process, and it is unlikely to be unambiguous-yet it is a high-stakes scientific achievement that will garner an enormous amount of public interest. Current and upcoming research efforts and missions aimed at detecting past and extant life could be supported by a consensus framework to plan for, assess and discuss life detection claims (c.f. Green et al., 2021). Such a framework could help increase the robustness of biosignature detection and interpretation, and improve communication with the scientific community and the public. In response to this need, and the call to the community to develop a confidence scale for standards of evidence for biosignature detection (Green et al., 2021), a community-organized workshop was held on July 19-22, 2021. The meeting was designed in a fully virtual (flipped) format. Preparatory materials including readings, instructional videos and activities were made available prior to the workshop, allowing the workshop schedule to be fully dedicated to active community discussion and prompted writing sessions. To maximize global interaction, the discussion components of the workshop were held during business hours in three different time zones, Asia/Pacific, European and US, with daily information hand-off between group organizers., Comment: 86 pages, 14 figures, workshop report

Published
2022

6. Physiological potential and evolutionary trajectories of syntrophic sulfate-reducing bacterial partners of anaerobic methanotrophic archaea

Author

Murali, Ranjani, Yu, Hang, Speth, Daan R, Wu, Fabai, Metcalfe, Kyle S, Crémière, Antoine, Laso-Pèrez, Rafael, Malmstrom, Rex R, Goudeau, Danielle, Woyke, Tanja, Hatzenpichler, Roland, Chadwick, Grayson L, Connon, Stephanie A, and Orphan, Victoria J

Subjects
Microbiology, Biological Sciences, Nutrition, Archaea, Anaerobiosis, Sulfates, Geologic Sediments, Bacteria, Oxidation-Reduction, Phylogeny, Agricultural and Veterinary Sciences, Medical and Health Sciences, Developmental Biology, Agricultural, veterinary and food sciences, Biological sciences, Biomedical and clinical sciences
Abstract

Sulfate-coupled anaerobic oxidation of methane (AOM) is performed by multicellular consortia of anaerobic methanotrophic archaea (ANME) in obligate syntrophic partnership with sulfate-reducing bacteria (SRB). Diverse ANME and SRB clades co-associate but the physiological basis for their adaptation and diversification is not well understood. In this work, we used comparative metagenomics and phylogenetics to investigate the metabolic adaptation among the 4 main syntrophic SRB clades (HotSeep-1, Seep-SRB2, Seep-SRB1a, and Seep-SRB1g) and identified features associated with their syntrophic lifestyle that distinguish them from their non-syntrophic evolutionary neighbors in the phylum Desulfobacterota. We show that the protein complexes involved in direct interspecies electron transfer (DIET) from ANME to the SRB outer membrane are conserved between the syntrophic lineages. In contrast, the proteins involved in electron transfer within the SRB inner membrane differ between clades, indicative of convergent evolution in the adaptation to a syntrophic lifestyle. Our analysis suggests that in most cases, this adaptation likely occurred after the acquisition of the DIET complexes in an ancestral clade and involve horizontal gene transfers within pathways for electron transfer (CbcBA) and biofilm formation (Pel). We also provide evidence for unique adaptations within syntrophic SRB clades, which vary depending on the archaeal partner. Among the most widespread syntrophic SRB, Seep-SRB1a, subclades that specifically partner ANME-2a are missing the cobalamin synthesis pathway, suggestive of nutritional dependency on its partner, while closely related Seep-SRB1a partners of ANME-2c lack nutritional auxotrophies. Our work provides insight into the features associated with DIET-based syntrophy and the adaptation of SRB towards it.

Published
2023

7. Thousands of small, novel genes predicted in global phage genomes

Author

Fremin, Brayon J, Bhatt, Ami S, Kyrpides, Nikos C, Consortium, Global Phage Small Open Reading Frame, Sengupta, Aditi, Sczyrba, Alexander, da Silva, Aline Maria, Buchan, Alison, Gaudin, Amelie, Brune, Andreas, Hirsch, Ann M, Neumann, Anthony, Shade, Ashley, Visel, Axel, Campbell, Barbara, Baker, Brett, Hedlund, Brian P, Crump, Byron C, Currie, Cameron, Kelly, Charlene, Craft, Chris, Hazard, Christina, Francis, Christopher, Schadt, Christopher W, Averill, Colin, Mobilian, Courtney, Buckley, Dan, Hunt, Dana, Noguera, Daniel, Beck, David, Valentine, David L, Walsh, David, Sumner, Dawn, Lymperopoulou, Despoina, Bhaya, Devaki, Bryant, Donald A, Morrison, Elise, Brodie, Eoin, Young, Erica, Lilleskov, Erik, Högfors-Rönnholm, Eva, Chen, Feng, Stewart, Frank, Nicol, Graeme W, Teeling, Hanno, Beller, Harry R, Dionisi, Hebe, Liao, Hui-Ling, Beman, J Michael, Stegen, James, Tiedje, James, Jansson, Janet, VanderGheynst, Jean, Norton, Jeanette, Dangl, Jeff, Blanchard, Jeffrey, Bowen, Jennifer, Macalady, Jennifer, Pett-Ridge, Jennifer, Rich, Jeremy, Payet, Jérôme P, Gladden, John D, Raff, Jonathan D, Klassen, Jonathan L, Tarn, Jonathan, Neufeld, Josh, Gravuer, Kelly, Hofmockel, Kirsten, Chen, Ko-Hsuan, Konstantinidis, Konstantinos, DeAngelis, Kristen M, Partida-Martinez, Laila P, Meredith, Laura, Chistoserdova, Ludmila, Moran, Mary Ann, Scarborough, Matthew, Schrenk, Matthew, Sullivan, Matthew, David, Maude, O'Malley, Michelle A, Medina, Monica, Habteselassie, Mussie, Ward, Nicholas D, Pietrasiak, Nicole, Mason, Olivia U, Sorensen, Patrick O, de los Santos, Paulina Estrada, Baldrian, Petr, McKay, R Michael, Simister, Rachel, Stepanauskas, Ramunas, Neumann, Rebecca, Malmstrom, Rex, Cavicchioli, Ricardo, Kelly, Robert, Hatzenpichler, Roland, Stocker, Roman, Cattolico, Rose Ann, Ziels, Ryan, and Vilgalys, Rytas

Subjects
Microbiology, Biological Sciences, Bioinformatics and Computational Biology, Genetics, Biotechnology, Human Genome, 2.1 Biological and endogenous factors, Generic health relevance, Bacteriophages, Genome, Viral, Genomics, Microbiota, Phylogeny, Global Phage Small Open Reading Frame (GP-SmORF) Consortium, CP: Microbiology, MetaRibo-Seq, comparative genomics, gene families, microbiome, phage, sORFs, small genes, Biochemistry and Cell Biology, Medical Physiology, Biological sciences
Abstract

Small genes (40,000 small-gene families in ∼2.3 million phage genome contigs. We find that small genes in phage genomes are approximately 3-fold more prevalent than in host prokaryotic genomes. Our approach enriches for small genes that are translated in microbiomes, suggesting the small genes identified are coding. More than 9,000 families encode potentially secreted or transmembrane proteins, more than 5,000 families encode predicted anti-CRISPR proteins, and more than 500 families encode predicted antimicrobial proteins. By combining homology and genomic-neighborhood analyses, we reveal substantial novelty and diversity within phage biology, including small phage genes found in multiple host phyla, small genes encoding proteins that play essential roles in host infection, and small genes that share genomic neighborhoods and whose encoded proteins may share related functions.

Published
2022

9. Metagenomes and Metagenome-Assembled Genomes from Substrate-Amended Hot Spring Sediment Incubations from Yellowstone National Park

Author

Reichart, Nicholas J, Bowers, Robert M, Woyke, Tanja, and Hatzenpichler, Roland

Subjects
Microbiology, Biological Sciences
Abstract

Here, we report on eight sediment metagenomes obtained from an alkaline hot spring, with their corresponding metagenome-assembled genomes. Samples had been incubated for 48 h with various substrate amendments in conjunction with the amino acid analog l-homopropargylglycine in a study targeted at identifying anabolicly active uncultured thermophilic archaea and bacteria.

Published
2022

10. Comparative genomics reveals electron transfer and syntrophic mechanisms differentiating methanotrophic and methanogenic archaea

Author

Chadwick, Grayson L, Skennerton, Connor T, Laso-Pérez, Rafael, Leu, Andy O, Speth, Daan R, Yu, Hang, Morgan-Lang, Connor, Hatzenpichler, Roland, Goudeau, Danielle, Malmstrom, Rex, Brazelton, William J, Woyke, Tanja, Hallam, Steven J, Tyson, Gene W, Wegener, Gunter, Boetius, Antje, and Orphan, Victoria J

Subjects
Microbiology, Biological Sciences, Genetics, Human Genome, Biotechnology, Anaerobiosis, Archaea, Electrons, Genomics, Geologic Sediments, Methane, Oxidation-Reduction, Phylogeny, Sulfates, Agricultural and Veterinary Sciences, Medical and Health Sciences, Developmental Biology, Agricultural, veterinary and food sciences, Biological sciences, Biomedical and clinical sciences
Abstract

The anaerobic oxidation of methane coupled to sulfate reduction is a microbially mediated process requiring a syntrophic partnership between anaerobic methanotrophic (ANME) archaea and sulfate-reducing bacteria (SRB). Based on genome taxonomy, ANME lineages are polyphyletic within the phylum Halobacterota, none of which have been isolated in pure culture. Here, we reconstruct 28 ANME genomes from environmental metagenomes and flow sorted syntrophic consortia. Together with a reanalysis of previously published datasets, these genomes enable a comparative analysis of all marine ANME clades. We review the genomic features that separate ANME from their methanogenic relatives and identify what differentiates ANME clades. Large multiheme cytochromes and bioenergetic complexes predicted to be involved in novel electron bifurcation reactions are well distributed and conserved in the ANME archaea, while significant variations in the anabolic C1 pathways exists between clades. Our analysis raises the possibility that methylotrophic methanogenesis may have evolved from a methanotrophic ancestor.

Published
2022

11. High Potential for Biomass-Degrading Enzymes Revealed by Hot Spring Metagenomics.

Author

Reichart, Nicholas, Bowers, Robert, Woyke, Tanja, and Hatzenpichler, Roland

Subjects
CAZyme, bioprospecting, biotechnology, cellulases, thermophilic enzymes
Abstract

Enzyme stability and activity at elevated temperatures are important aspects in biotechnological industries, such as the conversion of plant biomass into biofuels. In order to reduce the costs and increase the efficiency of biomass conversion, better enzymatic processing must be developed. Hot springs represent a treasure trove of underexplored microbiological and protein chemistry diversity. Herein, we conduct an exploratory study into the diversity of hot spring biomass-degrading potential. We describe the taxonomic diversity and carbohydrate active enzyme (CAZyme) coding potential in 71 publicly available metagenomic datasets from 58 globally distributed terrestrial geothermal features. Through taxonomic profiling, we detected a wide diversity of microbes unique to varying temperature and pH ranges. Biomass-degrading enzyme potential included all five classes of CAZymes and we described the presence or absence of genes encoding 19 glycosyl hydrolases hypothesized to be involved with cellulose, hemicellulose, and oligosaccharide degradation. Our results highlight hot springs as a promising system for the further discovery and development of thermo-stable biomass-degrading enzymes that can be applied toward generation of renewable biofuels. This study lays a foundation for future research to further investigate the functional diversity of hot spring biomass-degrading enzymes and their potential utility in biotechnological processing.

Published
2021

12. Roadmap for naming uncultivated Archaea and Bacteria

Author

Murray, Alison E, Freudenstein, John, Gribaldo, Simonetta, Hatzenpichler, Roland, Hugenholtz, Philip, Kämpfer, Peter, Konstantinidis, Konstantinos T, Lane, Christopher E, Papke, R Thane, Parks, Donovan H, Rossello-Mora, Ramon, Stott, Matthew B, Sutcliffe, Iain C, Thrash, J Cameron, Venter, Stephanus N, Whitman, William B, Acinas, Silvia G, Amann, Rudolf I, Anantharaman, Karthik, Armengaud, Jean, Baker, Brett J, Barco, Roman A, Bode, Helge B, Boyd, Eric S, Brady, Carrie L, Carini, Paul, Chain, Patrick SG, Colman, Daniel R, DeAngelis, Kristen M, de los Rios, Maria Asuncion, Estrada-de los Santos, Paulina, Dunlap, Christopher A, Eisen, Jonathan A, Emerson, David, Ettema, Thijs JG, Eveillard, Damien, Girguis, Peter R, Hentschel, Ute, Hollibaugh, James T, Hug, Laura A, Inskeep, William P, Ivanova, Elena P, Klenk, Hans-Peter, Li, Wen-Jun, Lloyd, Karen G, Löffler, Frank E, Makhalanyane, Thulani P, Moser, Duane P, Nunoura, Takuro, Palmer, Marike, Parro, Victor, Pedrós-Alió, Carlos, Probst, Alexander J, Smits, Theo HM, Steen, Andrew D, Steenkamp, Emma T, Spang, Anja, Stewart, Frank J, Tiedje, James M, Vandamme, Peter, Wagner, Michael, Wang, Feng-Ping, Yarza, Pablo, Hedlund, Brian P, and Reysenbach, Anna-Louise

Subjects
Microbiology, Biological Sciences, Ecology, Archaea, Bacteria, DNA, Bacterial, Metagenome, Phylogeny, Prokaryotic Cells, Sequence Analysis, DNA, Terminology as Topic, Medical Microbiology
Abstract

The assembly of single-amplified genomes (SAGs) and metagenome-assembled genomes (MAGs) has led to a surge in genome-based discoveries of members affiliated with Archaea and Bacteria, bringing with it a need to develop guidelines for nomenclature of uncultivated microorganisms. The International Code of Nomenclature of Prokaryotes (ICNP) only recognizes cultures as 'type material', thereby preventing the naming of uncultivated organisms. In this Consensus Statement, we propose two potential paths to solve this nomenclatural conundrum. One option is the adoption of previously proposed modifications to the ICNP to recognize DNA sequences as acceptable type material; the other option creates a nomenclatural code for uncultivated Archaea and Bacteria that could eventually be merged with the ICNP in the future. Regardless of the path taken, we believe that action is needed now within the scientific community to develop consistent rules for nomenclature of uncultivated taxa in order to provide clarity and stability, and to effectively communicate microbial diversity.

Published
2020

13. Common principles and best practices for engineering microbiomes

Author

Lawson, Christopher E, Harcombe, William R, Hatzenpichler, Roland, Lindemann, Stephen R, Löffler, Frank E, O’Malley, Michelle A, García Martín, Héctor, Pfleger, Brian F, Raskin, Lutgarde, Venturelli, Ophelia S, Weissbrodt, David G, Noguera, Daniel R, and McMahon, Katherine D

Subjects
Human Genome, Genetics, Affordable and Clean Energy, Agriculture, Bioelectric Energy Sources, Bioengineering, Biological Therapy, Environmental Microbiology, Guidelines as Topic, Humans, Microbiota, Practice Guidelines as Topic, Microbiology, Medical Microbiology
Abstract

Despite broad scientific interest in harnessing the power of Earth's microbiomes, knowledge gaps hinder their efficient use for addressing urgent societal and environmental challenges. We argue that structuring research and technology developments around a design-build-test-learn (DBTL) cycle will advance microbiome engineering and spur new discoveries of the basic scientific principles governing microbiome function. In this Review, we present key elements of an iterative DBTL cycle for microbiome engineering, focusing on generalizable approaches, including top-down and bottom-up design processes, synthetic and self-assembled construction methods, and emerging tools to analyse microbiome function. These approaches can be used to harness microbiomes for broad applications related to medicine, agriculture, energy and the environment. We also discuss key challenges and opportunities of each approach and synthesize them into best practice guidelines for engineering microbiomes. We anticipate that adoption of a DBTL framework will rapidly advance microbiome-based biotechnologies aimed at improving human and animal health, agriculture and enabling the bioeconomy.

Published
2019

14. Aerobic bacterial methane synthesis

Author

Wang, Qian, Alowaifeer, Abdullah, Kerner, Patricia, Balasubramanian, Narayanaganesh, Patterson, Angela, Christian, William, Tarver, Angela, Dore, John E., Hatzenpichler, Roland, Bothner, Brian, and McDermott, Timothy R.

Published
2021

17. Multicellular magnetotactic bacteria are genetically heterogeneous consortia with metabolically differentiated cells.

Author

Schaible, George, Schaible, George, Jay, Zackary, Cliff, John, Schulz, Frederik, Gauvin, Colin, Goudeau, Danielle, Malmstrom, Rex, Ruff, S, Edgcomb, Virginia, Hatzenpichler, Roland, Schaible, George, Schaible, George, Jay, Zackary, Cliff, John, Schulz, Frederik, Gauvin, Colin, Goudeau, Danielle, Malmstrom, Rex, Ruff, S, Edgcomb, Virginia, and Hatzenpichler, Roland

Abstract

Consortia of multicellular magnetotactic bacteria (MMB) are currently the only known example of bacteria without a unicellular stage in their life cycle. Because of their recalcitrance to cultivation, most previous studies of MMB have been limited to microscopic observations. To study the biology of these unique organisms in more detail, we use multiple culture-independent approaches to analyze the genomics and physiology of MMB consortia at single-cell resolution. We separately sequenced the metagenomes of 22 individual MMB consortia, representing 8 new species, and quantified the genetic diversity within each MMB consortium. This revealed that, counter to conventional views, cells within MMB consortia are not clonal. Single consortia metagenomes were then used to reconstruct the species-specific metabolic potential and infer the physiological capabilities of MMB. To validate genomic predictions, we performed stable isotope probing (SIP) experiments and interrogated MMB consortia using fluorescence in situ hybridization (FISH) combined with nanoscale secondary ion mass spectrometry (NanoSIMS). By coupling FISH with bioorthogonal noncanonical amino acid tagging (BONCAT), we explored their in situ activity as well as variation of protein synthesis within cells. We demonstrate that MMB consortia are mixotrophic sulfate reducers and that they exhibit metabolic differentiation between individual cells, suggesting that MMB consortia are more complex than previously thought. These findings expand our understanding of MMB diversity, ecology, genomics, and physiology, as well as offer insights into the mechanisms underpinning the multicellular nature of their unique lifestyle.

Published
2024

18. Diversity and evolution of nitric oxide reduction in bacteria and archaea.

Author

Murali, Ranjani, Pace, Laura A., Sanford, Robert A., Ward, L. M., Lynes, Mackenzie M., Hatzenpichler, Roland, Lingappa, Usha F., Fischer, Woodward W., Gennis, Robert B., and Hemp, James

Subjects
NITRIC oxide, ARCHAEBACTERIA, ENERGY conservation, NITROUS oxide, BACTERIA
Abstract

Nitrous oxide is a potent greenhouse gas whose production is catalyzed by nitric oxide reductase (NOR) members of the heme-copper oxidoreductase (HCO) enzyme superfamily. We identified several previously uncharacterized HCO families, four of which (eNOR, sNOR, gNOR, and nNOR) appear to perform NO reduction. These families have novel active-site structures and several have conserved proton channels, suggesting that they might be able to couple NO reduction to energy conservation. We isolated and biochemically characterized a member of the eNOR family from the bacterium Rhodothermus marinus and found that it performs NO reduction. These recently identified NORs exhibited broad phylogenetic and environmental distributions, greatly expanding the diversity of microbes in nature capable of NO reduction. Phylogenetic analyses further demonstrated that NORs evolved multiple times independently from oxygen reductases, supporting the view that complete denitrification evolved after aerobic respiration. [ABSTRACT FROM AUTHOR]

Published
2024
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20. Visualizing in situ translational activity for identifying and sorting slow-growing archaeal−bacterial consortia

Author

Hatzenpichler, Roland, Connon, Stephanie A, Goudeau, Danielle, Malmstrom, Rex R, Woyke, Tanja, and Orphan, Victoria J

Subjects
Microbiology, Biological Sciences, Genetics, Life Below Water, Alkynes, Anaerobiosis, Archaea, Bacteria, Environmental Microbiology, Flow Cytometry, Geologic Sediments, Glycine, Methane, Microbial Consortia, Protein Biosynthesis, Staining and Labeling, activity-based cell sorting, BONCAT, click chemistry, ecophysiology, single-cell microbiology
Abstract

To understand the biogeochemical roles of microorganisms in the environment, it is important to determine when and under which conditions they are metabolically active. Bioorthogonal noncanonical amino acid tagging (BONCAT) can reveal active cells by tracking the incorporation of synthetic amino acids into newly synthesized proteins. The phylogenetic identity of translationally active cells can be determined by combining BONCAT with rRNA-targeted fluorescence in situ hybridization (BONCAT-FISH). In theory, BONCAT-labeled cells could be isolated with fluorescence-activated cell sorting (BONCAT-FACS) for subsequent genetic analyses. Here, in the first application, to our knowledge, of BONCAT-FISH and BONCAT-FACS within an environmental context, we probe the translational activity of microbial consortia catalyzing the anaerobic oxidation of methane (AOM), a dominant sink of methane in the ocean. These consortia, which typically are composed of anaerobic methane-oxidizing archaea (ANME) and sulfate-reducing bacteria, have been difficult to study due to their slow in situ growth rates, and fundamental questions remain about their ecology and diversity of interactions occurring between ANME and associated partners. Our activity-correlated analyses of >16,400 microbial aggregates provide the first evidence, to our knowledge, that AOM consortia affiliated with all five major ANME clades are concurrently active under controlled conditions. Surprisingly, sorting of individual BONCAT-labeled consortia followed by whole-genome amplification and 16S rRNA gene sequencing revealed previously unrecognized interactions of ANME with members of the poorly understood phylum Verrucomicrobia This finding, together with our observation that ANME-associated Verrucomicrobia are found in a variety of geographically distinct methane seep environments, suggests a broader range of symbiotic relationships within AOM consortia than previously thought.

Published
2016

21. Visualizing in situ translational activity for identifying and sorting slow-growing archaeal-bacterial consortia.

Author

Hatzenpichler, Roland, Connon, Stephanie A, Goudeau, Danielle, Malmstrom, Rex R, Woyke, Tanja, and Orphan, Victoria J

Subjects
Bacteria, Archaea, Methane, Alkynes, Glycine, Flow Cytometry, Staining and Labeling, Environmental Microbiology, Protein Biosynthesis, Anaerobiosis, Geologic Sediments, Microbial Consortia, BONCAT, activity-based cell sorting, click chemistry, ecophysiology, single-cell microbiology
Abstract

To understand the biogeochemical roles of microorganisms in the environment, it is important to determine when and under which conditions they are metabolically active. Bioorthogonal noncanonical amino acid tagging (BONCAT) can reveal active cells by tracking the incorporation of synthetic amino acids into newly synthesized proteins. The phylogenetic identity of translationally active cells can be determined by combining BONCAT with rRNA-targeted fluorescence in situ hybridization (BONCAT-FISH). In theory, BONCAT-labeled cells could be isolated with fluorescence-activated cell sorting (BONCAT-FACS) for subsequent genetic analyses. Here, in the first application, to our knowledge, of BONCAT-FISH and BONCAT-FACS within an environmental context, we probe the translational activity of microbial consortia catalyzing the anaerobic oxidation of methane (AOM), a dominant sink of methane in the ocean. These consortia, which typically are composed of anaerobic methane-oxidizing archaea (ANME) and sulfate-reducing bacteria, have been difficult to study due to their slow in situ growth rates, and fundamental questions remain about their ecology and diversity of interactions occurring between ANME and associated partners. Our activity-correlated analyses of >16,400 microbial aggregates provide the first evidence, to our knowledge, that AOM consortia affiliated with all five major ANME clades are concurrently active under controlled conditions. Surprisingly, sorting of individual BONCAT-labeled consortia followed by whole-genome amplification and 16S rRNA gene sequencing revealed previously unrecognized interactions of ANME with members of the poorly understood phylum Verrucomicrobia This finding, together with our observation that ANME-associated Verrucomicrobia are found in a variety of geographically distinct methane seep environments, suggests a broader range of symbiotic relationships within AOM consortia than previously thought.

Published
2016

28. Unraveling the functional dark matter through global metagenomics

Author

Pavlopoulos, Georgios A., Baltoumas, Fotis A., Liu, Sirui, Selvitopi, Oguz, Camargo, Antonio Pedro, Nayfach, Stephen, Azad, Ariful, Roux, Simon, Call, Lee, Ivanova, Natalia N., Chen, I. Min, Paez-Espino, David, Karatzas, Evangelos, Acinas, Silvia G., Ahlgren, Nathan, Attwood, Graeme, Baldrian, Petr, Berry, Timothy, Bhatnagar, Jennifer M., Bhaya, Devaki, Bidle, Kay D., Blanchard, Jeffrey L., Boyd, Eric S., Bowen, Jennifer L., Bowman, Jeff, Brawley, Susan H., Brodie, Eoin L., Brune, Andreas, Bryant, Donald A., Buchan, Alison, Cadillo-Quiroz, Hinsby, Campbell, Barbara J., Cavicchioli, Ricardo, Chuckran, Peter F., Coleman, Maureen, Crowe, Sean, Colman, Daniel R., Currie, Cameron R., Dangl, Jeff, Delherbe, Nathalie, Denef, Vincent J., Dijkstra, Paul, Distel, Daniel D., Eloe-Fadrosh, Emiley, Fisher, Kirsten, Francis, Christopher, Garoutte, Aaron, Gaudin, Amelie, Gerwick, Lena, Godoy-Vitorino, Filipa, Guerra, Peter, Guo, Jiarong, Habteselassie, Mussie Y., Hallam, Steven J., Hatzenpichler, Roland, Hentschel, Ute, Hess, Matthias, Hirsch, Ann M., Hug, Laura A., Hultman, Jenni, Hunt, Dana E., Huntemann, Marcel, Inskeep, William P., James, Timothy Y., Jansson, Janet, Johnston, Eric R., Kalyuzhnaya, Marina, Kelly, Charlene N., Kelly, Robert M., Klassen, Jonathan L., Nüsslein, Klaus, Kostka, Joel E., Lindow, Steven, Lilleskov, Erik, Lynes, Mackenzie, Mackelprang, Rachel, Martin, Francis M., Mason, Olivia U., McKay, R. Michael, McMahon, Katherine, Mead, David A., Medina, Monica, Meredith, Laura K., Mock, Thomas, Mohn, William W., Moran, Mary Ann, Murray, Alison, Neufeld, Josh D., Neumann, Rebecca, Norton, Jeanette M., Partida-Martinez, Laila P., Pietrasiak, Nicole, Pelletier, Dale, Reddy, T. B. K., Reese, Brandi Kiel, Reichart, Nicholas J., Reiss, Rebecca, Saito, Mak A., Schachtman, Daniel P., Seshadri, Rekha, Shade, Ashley, Sherman, David, Simister, Rachel, Simon, Holly, Stegen, James, Stepanauskas, Ramunas, Sullivan, Matthew, Sumner, Dawn Y., Teeling, Hanno, Thamatrakoln, Kimberlee, Treseder, Kathleen, Tringe, Susannah, Vaishampayan, Parag, Valentine, David L., Waldo, Nicholas B., Waldrop, Mark P., Walsh, David A., Ward, David M., Wilkins, Michael, Whitman, Thea, Woolet, Jamie, Woyke, Tanja, Iliopoulos, Ioannis, Konstantinidis, Konstantinos, Tiedje, James M., Pett-Ridge, Jennifer, Baker, David, Visel, Axel, Ouzounis, Christos A., Ovchinnikov, Sergey, Buluç, Aydin, Kyrpides, Nikos C., Pavlopoulos, Georgios A., Baltoumas, Fotis A., Liu, Sirui, Selvitopi, Oguz, Camargo, Antonio Pedro, Nayfach, Stephen, Azad, Ariful, Roux, Simon, Call, Lee, Ivanova, Natalia N., Chen, I. Min, Paez-Espino, David, Karatzas, Evangelos, Acinas, Silvia G., Ahlgren, Nathan, Attwood, Graeme, Baldrian, Petr, Berry, Timothy, Bhatnagar, Jennifer M., Bhaya, Devaki, Bidle, Kay D., Blanchard, Jeffrey L., Boyd, Eric S., Bowen, Jennifer L., Bowman, Jeff, Brawley, Susan H., Brodie, Eoin L., Brune, Andreas, Bryant, Donald A., Buchan, Alison, Cadillo-Quiroz, Hinsby, Campbell, Barbara J., Cavicchioli, Ricardo, Chuckran, Peter F., Coleman, Maureen, Crowe, Sean, Colman, Daniel R., Currie, Cameron R., Dangl, Jeff, Delherbe, Nathalie, Denef, Vincent J., Dijkstra, Paul, Distel, Daniel D., Eloe-Fadrosh, Emiley, Fisher, Kirsten, Francis, Christopher, Garoutte, Aaron, Gaudin, Amelie, Gerwick, Lena, Godoy-Vitorino, Filipa, Guerra, Peter, Guo, Jiarong, Habteselassie, Mussie Y., Hallam, Steven J., Hatzenpichler, Roland, Hentschel, Ute, Hess, Matthias, Hirsch, Ann M., Hug, Laura A., Hultman, Jenni, Hunt, Dana E., Huntemann, Marcel, Inskeep, William P., James, Timothy Y., Jansson, Janet, Johnston, Eric R., Kalyuzhnaya, Marina, Kelly, Charlene N., Kelly, Robert M., Klassen, Jonathan L., Nüsslein, Klaus, Kostka, Joel E., Lindow, Steven, Lilleskov, Erik, Lynes, Mackenzie, Mackelprang, Rachel, Martin, Francis M., Mason, Olivia U., McKay, R. Michael, McMahon, Katherine, Mead, David A., Medina, Monica, Meredith, Laura K., Mock, Thomas, Mohn, William W., Moran, Mary Ann, Murray, Alison, Neufeld, Josh D., Neumann, Rebecca, Norton, Jeanette M., Partida-Martinez, Laila P., Pietrasiak, Nicole, Pelletier, Dale, Reddy, T. B. K., Reese, Brandi Kiel, Reichart, Nicholas J., Reiss, Rebecca, Saito, Mak A., Schachtman, Daniel P., Seshadri, Rekha, Shade, Ashley, Sherman, David, Simister, Rachel, Simon, Holly, Stegen, James, Stepanauskas, Ramunas, Sullivan, Matthew, Sumner, Dawn Y., Teeling, Hanno, Thamatrakoln, Kimberlee, Treseder, Kathleen, Tringe, Susannah, Vaishampayan, Parag, Valentine, David L., Waldo, Nicholas B., Waldrop, Mark P., Walsh, David A., Ward, David M., Wilkins, Michael, Whitman, Thea, Woolet, Jamie, Woyke, Tanja, Iliopoulos, Ioannis, Konstantinidis, Konstantinos, Tiedje, James M., Pett-Ridge, Jennifer, Baker, David, Visel, Axel, Ouzounis, Christos A., Ovchinnikov, Sergey, Buluç, Aydin, and Kyrpides, Nikos C.

Abstract

Metagenomes encode an enormous diversity of proteins, reflecting a multiplicity of functions and activities1,2. Exploration of this vast sequence space has been limited to a comparative analysis against reference microbial genomes and protein families derived from those genomes. Here, to examine the scale of yet untapped functional diversity beyond what is currently possible through the lens of reference genomes, we develop a computational approach to generate reference-free protein families from the sequence space in metagenomes. We analyse 26,931 metagenomes and identify 1.17 billion protein sequences longer than 35 amino acids with no similarity to any sequences from 102,491 reference genomes or the Pfam database3. Using massively parallel graph-based clustering, we group these proteins into 106,198 novel sequence clusters with more than 100 members, doubling the number of protein families obtained from the reference genomes clustered using the same approach. We annotate these families on the basis of their taxonomic, habitat, geographical and gene neighbourhood distributions and, where sufficient sequence diversity is available, predict protein three-dimensional models, revealing novel structures. Overall, our results uncover an enormously diverse functional space, highlighting the importance of further exploring the microbial functional dark matter.

Published
2023
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29. Physiological potential and evolutionary trajectories of syntrophic sulfate-reducing bacterial partners of anaerobic methanotrophic archaea

Author

Laso-Pérez, Rafael [0000-0002-6912-7865], Murali, Ranjani, Yu, Hang, Speth, Daan R., Wu, Fabai, Metcalfe, Kyle S., Crémière, Antoine, Laso-Pérez, Rafael, Malmstrom, Rex R., Goudeau, Danielle, Woyke, Tanja, Hatzenpichler, Roland, Chadwick, Grayson L., Connon, Stephanie A., Orphan, Victoria J., Laso-Pérez, Rafael [0000-0002-6912-7865], Murali, Ranjani, Yu, Hang, Speth, Daan R., Wu, Fabai, Metcalfe, Kyle S., Crémière, Antoine, Laso-Pérez, Rafael, Malmstrom, Rex R., Goudeau, Danielle, Woyke, Tanja, Hatzenpichler, Roland, Chadwick, Grayson L., Connon, Stephanie A., and Orphan, Victoria J.

Abstract

Sulfate-coupled anaerobic oxidation of methane (AOM) is performed by multicellular consortia of anaerobic methanotrophic archaea (ANME) in obligate syntrophic partnership with sulfate-reducing bacteria (SRB). Diverse ANME and SRB clades co-associate but the physiological basis for their adaptation and diversification is not well understood. In this work, we used comparative metagenomics and phylogenetics to investigate the metabolic adaptation among the 4 main syntrophic SRB clades (HotSeep-1, Seep-SRB2, Seep-SRB1a, and Seep-SRB1g) and identified features associated with their syntrophic lifestyle that distinguish them from their non-syntrophic evolutionary neighbors in the phylum Desulfobacterota. We show that the protein complexes involved in direct interspecies electron transfer (DIET) from ANME to the SRB outer membrane are conserved between the syntrophic lineages. In contrast, the proteins involved in electron transfer within the SRB inner membrane differ between clades, indicative of convergent evolution in the adaptation to a syntrophic lifestyle. Our analysis suggests that in most cases, this adaptation likely occurred after the acquisition of the DIET complexes in an ancestral clade and involve horizontal gene transfers within pathways for electron transfer (CbcBA) and biofilm formation (Pel). We also provide evidence for unique adaptations within syntrophic SRB clades, which vary depending on the archaeal partner. Among the most widespread syntrophic SRB, Seep-SRB1a, subclades that specifically partner ANME-2a are missing the cobalamin synthesis pathway, suggestive of nutritional dependency on its partner, while closely related Seep-SRB1a partners of ANME-2c lack nutritional auxotrophies. Our work provides insight into the features associated with DIET-based syntrophy and the adaptation of SRB towards it.

Published
2023

31. Author Correction: Roadmap for naming uncultivated Archaea and Bacteria

Author

Murray, Alison E., Freudenstein, John, Gribaldo, Simonetta, Hatzenpichler, Roland, Hugenholtz, Philip, Kämpfer, Peter, Konstantinidis, Konstantinos T., Lane, Christopher E., Papke, R. Thane, Parks, Donovan H., Rossello-Mora, Ramon, Stott, Matthew B., Sutcliffe, Iain C., Thrash, J. Cameron, Venter, Stephanus N., Whitman, William B., Acinas, Silvia G., Amann, Rudolf I., Anantharaman, Karthik, Armengaud, Jean, Baker, Brett J., Barco, Roman A., Bode, Helge B., Boyd, Eric S., Brady, Carrie L., Carini, Paul, Chain, Patrick S. G., Colman, Daniel R., DeAngelis, Kristen M., de los Rios, Maria Asuncion, Estrada-de los Santos, Paulina, Dunlap, Christopher A., Eisen, Jonathan A., Emerson, David, Ettema, Thijs J. G., Eveillard, Damien, Girguis, Peter R., Hentschel, Ute, Hollibaugh, James T., Hug, Laura A., Inskeep, William P., Ivanova, Elena P., Klenk, Hans-Peter, Li, Wen-Jun, Lloyd, Karen G., Löffler, Frank E., Makhalanyane, Thulani P., Moser, Duane P., Nunoura, Takuro, Palmer, Marike, Parro, Victor, Pedrós-Alió, Carlos, Probst, Alexander J., Smits, Theo H. M., Steen, Andrew D., Steenkamp, Emma T., Spang, Anja, Stewart, Frank J., Tiedje, James M., Vandamme, Peter, Wagner, Michael, Wang, Feng-Ping, Yarza, Pablo, Hedlund, Brian P., and Reysenbach, Anna-Louise

Published
2021
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32. Physiological adaptation of sulfate reducing bacteria in syntrophic partnership with anaerobic methanotrophic archaea

Author

Murali, Ranjani, primary, Yu, Hang, additional, Speth, Daan R., additional, Wu, Fabai, additional, Metcalfe, Kyle S., additional, Crémière, Antoine, additional, Laso-Pèrez, Rafael, additional, Malmstrom, Rex R., additional, Goudeau, Danielle, additional, Woyke, Tanja, additional, Hatzenpichler, Roland, additional, Chadwick, Grayson L., additional, and Orphan, Victoria J., additional

Published
2022
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36. Comparative genomics reveals electron transfer and syntrophic mechanisms differentiating methanotrophic and methanogenic archaea

Author

Chadwick, Grayson L., Skennerton, Connor T., Laso-Pérez, Rafael, Leu, Andy O., Speth, Daan R., Yu, Hang, Morgan-Lang, Connor, Hatzenpichler, Roland, Goudeau, Danielle, Malmstrom, Rex, Brazelton, William J., Woyke, Tanja, Hallam, Steven J., Tyson, Gene W., Wegener, Gunter, Boetius, Antje, Orphan, Victoria J., Chadwick, Grayson L., Skennerton, Connor T., Laso-Pérez, Rafael, Leu, Andy O., Speth, Daan R., Yu, Hang, Morgan-Lang, Connor, Hatzenpichler, Roland, Goudeau, Danielle, Malmstrom, Rex, Brazelton, William J., Woyke, Tanja, Hallam, Steven J., Tyson, Gene W., Wegener, Gunter, Boetius, Antje, and Orphan, Victoria J.

Abstract

The anaerobic oxidation of methane coupled to sulfate reduction is a microbially mediated process requiring a syntrophic partnership between anaerobic methanotrophic (ANME) archaea and sulfate-reducing bacteria (SRB). Based on genome taxonomy, ANME lineages are polyphyletic within the phylum Halobacterota, none of which have been isolated in pure culture. Here, we reconstruct 28 ANME genomes from environmental metagenomes and flow sorted syntrophic consortia. Together with a reanalysis of previously published datasets, these genomes enable a comparative analysis of all marine ANME clades. We review the genomic features that separate ANME from their methanogenic relatives and identify what differentiates ANME clades. Large multiheme cytochromes and bioenergetic complexes predicted to be involved in novel electron bifurcation reactions are well distributed and conserved in the ANME archaea, while significant variations in the anabolic C1 pathways exists between clades. Our analysis raises the possibility that methylotrophic methanogenesis may have evolved from a methanotrophic ancestor.

Published
2022

37. Physiological adaptation of sulfate reducing bacteria in syntrophic partnership with anaerobic methanotrophic archaea

Author

Murali, Ranjani, Yu, Hang, Speth, Daan R., Wu, Fabai, Metcalfe, Kyle S., Crémière, Antoine, Laso-Pérez, Rafael, Malmstrom, Rex R., Goudeau, Danielle, Woyke, Tanja, Hatzenpichler, Roland, Chadwick, Grayson L., Orphan, Victoria J., Murali, Ranjani, Yu, Hang, Speth, Daan R., Wu, Fabai, Metcalfe, Kyle S., Crémière, Antoine, Laso-Pérez, Rafael, Malmstrom, Rex R., Goudeau, Danielle, Woyke, Tanja, Hatzenpichler, Roland, Chadwick, Grayson L., and Orphan, Victoria J.

Abstract

Sulfate-coupled anaerobic oxidation of methane (AOM) is performed by multicellular consortia of anaerobic methanotrophic archaea (ANME) in obligate syntrophic partnership with sulfate-reducing bacteria (SRB). Diverse ANME and SRB clades co-associate but the physiological basis for their adaptation and diversification is not well understood. In this work, we explore the metabolic adaptation of four syntrophic SRB clades (HotSeep-1, Seep-SRB2, Seep-SRB1a and Seep-SRB1g) from a phylogenomics perspective, tracing the evolution of conserved proteins in the syntrophic SRB clades, and comparing the genomes of syntrophic SRB to their nearest evolutionary neighbors in the phylum Desulfobacterota. We note several examples of gain, loss or biochemical adaptation of proteins within pathways involved in extracellular electron transfer, electron transport chain, nutrient sharing, biofilm formation and cell adhesion. We demonstrate that the metabolic adaptations in each of these syntrophic clades are unique, suggesting that they have independently evolved, converging to a syntrophic partnership with ANME. Within the clades we also investigated the specialization of different syntrophic SRB species to partnerships with different ANME clades, using metagenomic sequences obtained from ANME and SRB partners in individual consortia after fluorescent-sorting of cell aggregates from anaerobic sediments. In one instance of metabolic adaptation to different partnerships, we show that Seep-SRB1a partners of ANME-2c appear to lack nutritional auxotrophies, while the related Seep-SRB1a partners of a different methanotrophic archaeal lineage, ANME-2a, are missing the cobalamin synthesis pathway, suggesting that the Seep-SRB1a partners of ANME-2a may have a nutritional dependence on its partner. Together, our paired genomic analysis of AOM consortia highlights the specific adaptation and diversification of syntrophic SRB clades linked to their associated ANME lineages.

Published
2022

38. Comparative genomics reveals electron transfer and syntrophic mechanisms differentiating methanotrophic and methanogenic archaea

Author

Laso-Pérez, Rafael [0000-0002-6912-7865], Chadwick, Grayson L, Skennerton, Connor T, Laso-Pérez, Rafael, Leu, Andy O, Speth, Daan R, Yu, Hang, Morgan-Lang, Connor, Hatzenpichler, Roland, Goudeau, Danielle, Malmstrom, Rex, Brazelton, William J, Woyke, Tanja, Hallam, Steven J, Tyson, Gene W, Wegener, Gunter, Boetius, Antje, Orphan, Victoria J, Laso-Pérez, Rafael [0000-0002-6912-7865], Chadwick, Grayson L, Skennerton, Connor T, Laso-Pérez, Rafael, Leu, Andy O, Speth, Daan R, Yu, Hang, Morgan-Lang, Connor, Hatzenpichler, Roland, Goudeau, Danielle, Malmstrom, Rex, Brazelton, William J, Woyke, Tanja, Hallam, Steven J, Tyson, Gene W, Wegener, Gunter, Boetius, Antje, and Orphan, Victoria J

Abstract

The anaerobic oxidation of methane coupled to sulfate reduction is a microbially mediated process requiring a syntrophic partnership between anaerobic methanotrophic (ANME) archaea and sulfate-reducing bacteria (SRB). Based on genome taxonomy, ANME lineages are polyphyletic within the phylum Halobacterota, none of which have been isolated in pure culture. Here, we reconstruct 28 ANME genomes from environmental metagenomes and flow sorted syntrophic consortia. Together with a reanalysis of previously published datasets, these genomes enable a comparative analysis of all marine ANME clades. We review the genomic features that separate ANME from their methanogenic relatives and identify what differentiates ANME clades. Large multiheme cytochromes and bioenergetic complexes predicted to be involved in novel electron bifurcation reactions are well distributed and conserved in the ANME archaea, while significant variations in the anabolic C1 pathways exists between clades. Our analysis raises the possibility that methylotrophic methanogenesis may have evolved from a methanotrophic ancestor.

Published
2022

46. Diversity and evolution of nitric oxide reduction

Author

Murali, Ranjani, primary, Pace, Laura A., additional, Sanford, Robert A., additional, Ward, Lewis M., additional, Lynes, Mackenzie, additional, Hatzenpichler, Roland, additional, Lingappa, Usha F., additional, Fischer, Woodward W., additional, Gennis, Robert B., additional, and Hemp, James, additional

Published
2021
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47. Comparative genomics reveals electron transfer and syntrophic mechanisms differentiating methanotrophic and methanogenic archaea

Author

Chadwick, Grayson L, primary, Skennerton, Connor T, additional, Laso-Pérez, Rafael, additional, Leu, Andy O, additional, Speth, Daan R, additional, Yu, Hang, additional, Morgan-Lang, Connor, additional, Hatzenpichler, Roland, additional, Goudeau, Danielle, additional, Malmstrom, Rex, additional, Brazelton, William J, additional, Woyke, Tanja, additional, Hallam, Steven J, additional, Tyson, Gene W, additional, Wegener, Gunter, additional, Boetius, Antje, additional, and Orphan, Victoria J, additional

Published
2021
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49. Comparative genomics reveals electron transfer and syntrophic mechanisms differentiating methanotrophic and methanogenic archaea

Author

Chadwick, Grayson L., Skennerton, Connor T., Laso-Pérez, Rafael, Leu, Andy O., Speth, Daan R., Yu, Hang, Morgan-Lang, Connor, Hatzenpichler, Roland, Goudeau, Danielle, Malmstrom, Rex, Brazelton, William J., Woyke, Tanja, Hallam, Steven J., Tyson, Gene W., Wegener, Gunter, Boetius, Antje, Orphan, Victoria Jeanne, Chadwick, Grayson L., Skennerton, Connor T., Laso-Pérez, Rafael, Leu, Andy O., Speth, Daan R., Yu, Hang, Morgan-Lang, Connor, Hatzenpichler, Roland, Goudeau, Danielle, Malmstrom, Rex, Brazelton, William J., Woyke, Tanja, Hallam, Steven J., Tyson, Gene W., Wegener, Gunter, Boetius, Antje, and Orphan, Victoria Jeanne

Abstract

The anaerobic oxidation of methane coupled to sulfate reduction is a microbially mediated process requiring a syntrophic partnership between anaerobic methanotrophic (ANME) archaea and sulfate reducing bacteria (SRB). Based on genome taxonomy, ANME lineages are polyphyletic within the phylum Halobacterota, none of which have been isolated in pure culture. Here we reconstruct 28 ANME genomes from environmental metagenomes and flow sorted syntrophic consortia. Together with a reanalysis of previously published datasets, these genomes enable a comparative analysis of all marine ANME clades. We review the genomic features which separate ANME from their methanogenic relatives and identify what differentiates ANME clades. Large multiheme cytochromes and bioenergetic complexes predicted to be involved in novel electron bifurcation reactions are well-distributed and conserved in the ANME archaea, while significant variations in the anabolic C1 pathways exists between clades. Our analysis raises the possibility that methylotrophic methanogenesis may have evolved from a methanotrophic ancestor.

Published
2021

50. 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

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