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2. Biosynthesis of chlorophyll c in a dinoflagellate and heterologous production in planta

Author

Jinkerson, Robert E, Poveda-Huertes, Daniel, Cooney, Elizabeth C, Cho, Anna, Ochoa-Fernandez, Rocio, Keeling, Patrick J, Xiang, Tingting, and Andersen-Ranberg, Johan

Subjects
Plant Biology, Biological Sciences, Chlorophyll A, Chlorophyll, Proteins, Plants, Dinoflagellida, Phylogeny, oxoglutarate-Fe(II) dioxygenase, Breviolum minutum, CHLCS, CHLOROPHYLL C SYNTHASE, biosynthesis, chlorophyll c, chromalveolate, dinoflagellate, Medical and Health Sciences, Psychology and Cognitive Sciences, Developmental Biology, Biological sciences, Biomedical and clinical sciences, Psychology
Abstract

Chlorophyll c is a key photosynthetic pigment that has been used historically to classify eukaryotic algae. Despite its importance in global photosynthetic productivity, the pathway for its biosynthesis has remained elusive. Here we define the CHLOROPHYLL C SYNTHASE (CHLCS) discovered through investigation of a dinoflagellate mutant deficient in chlorophyll c. CHLCSs are proteins with chlorophyll a/b binding and 2-oxoglutarate-Fe(II) dioxygenase (2OGD) domains found in peridinin-containing dinoflagellates; other chlorophyll c-containing algae utilize enzymes with only the 2OGD domain or an unknown synthase to produce chlorophyll c. 2OGD-containing synthases across dinoflagellate, diatom, cryptophyte, and haptophyte lineages form a monophyletic group, 8 members of which were also shown to produce chlorophyll c. Chlorophyll c1 to c2 ratios in marine algae are dictated in part by chlorophyll c synthases. CHLCS heterologously expressed in planta results in the accumulation of chlorophyll c1 and c2, demonstrating a path to augment plant pigment composition with algal counterparts.

Published
2024

4. The microbiome of a bacterivorous marine choanoflagellate contains a resource-demanding obligate bacterial associate

Author

Needham, David M, Poirier, Camille, Bachy, Charles, George, Emma E, Wilken, Susanne, Yung, Charmaine CM, Limardo, Alexander J, Morando, Michael, Sudek, Lisa, Malmstrom, Rex R, Keeling, Patrick J, Santoro, Alyson E, and Worden, Alexandra Z

Subjects
Microbiology, Biological Sciences, Emerging Infectious Diseases, Microbiome, Infectious Diseases, Infection, Life Below Water, Animals, Bacteria, Choanoflagellata, Humans, Microbiota, Pacific Ocean, Type IV Secretion Systems, Medical Microbiology
Abstract

Microbial predators such as choanoflagellates are key players in ocean food webs. Choanoflagellates, which are the closest unicellular relatives of animals, consume bacteria and also exhibit marked biological transitions triggered by bacterial compounds, yet their native microbiomes remain uncharacterized. Here we report the discovery of a ubiquitous, uncultured bacterial lineage we name Candidatus Comchoanobacterales ord. nov., related to the human pathogen Coxiella and physically associated with the uncultured marine choanoflagellate Bicosta minor. We analyse complete 'Comchoano' genomes acquired after sorting single Bicosta cells, finding signatures of obligate host-dependence, including reduction of pathways encoding glycolysis, membrane components, amino acids and B-vitamins. Comchoano encode the necessary apparatus to import energy and other compounds from the host, proteins for host-cell associations and a type IV secretion system closest to Coxiella's that is expressed in Pacific Ocean metatranscriptomes. Interactions between choanoflagellates and their microbiota could reshape the direction of energy and resource flow attributed to microbial predators, adding complexity and nuance to marine food webs.

Published
2022

5. A computational framework for modelling infectious disease policy based on age and household structure with applications to the COVID-19 pandemic

Author

Hilton, Joe, Riley, Heather, Pellis, Lorenzo, Aziza, Rabia, Brand, Samuel P. C., Kombe, Ivy K., Ojal, John, Parisi, Andrea, Keeling, Matt J., Nokes, D. James, Manson-Sawko, Robert, and House, Thomas

Subjects
Quantitative Biology - Populations and Evolution, Statistics - Other Statistics
Abstract

The widespread, and in many countries unprecedented, use of non-pharmaceutical interventions (NPIs) during the COVID-19 pandemic has highlighted the need for mathematical models which can estimate the impact of these measures while accounting for the highly heterogeneous risk profile of COVID-19. Models accounting either for age structure or the household structure necessary to explicitly model many NPIs are commonly used in infectious disease modelling, but models incorporating both levels of structure present substantial computational and mathematical challenges due to their high dimensionality. Here we present a modelling framework for the spread of an epidemic that includes explicit representation of age structure and household structure. Our model is formulated in terms of tractable systems of ordinary differential equations for which we provide an open-source Python implementation. Such tractability leads to significant benefits for model calibration, exhaustive evaluation of possible parameter values, and interpretability of results. We demonstrate the flexibility of our model through four policy case studies, where we quantify the likely benefits of the following measures which were either considered or implemented in the UK during the current COVID-19 pandemic: control of within- and between-household mixing through NPIs; formation of support bubbles during lockdown periods; out-of-household isolation (OOHI); and temporary relaxation of NPIs during holiday periods. Our ordinary differential equation formulation and associated analysis demonstrate that multiple dimensions of risk stratification and social structure can be incorporated into infectious disease models without sacrificing mathematical tractability. This model and its software implementation expand the range of tools available to infectious disease policy analysts., Comment: 45 pages, 9 figures

Published
2022
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12. Single cell transcriptomics of ABEDINIUM reveals a new early-branching dinoflagellate lineage

Author

Cooney, Elizabeth C, Okamoto, Noriko, Cho, Anna, Hehenberger, Elisabeth, Richards, Thomas A, Santoro, Alyson E, Worden, Alexandra Z, Leander, Brian S, and Keeling, Patrick J

Subjects
Emerging Infectious Diseases, Infectious Diseases, Genetics, Human Genome, 1.1 Normal biological development and functioning, Underpinning research, Dinoflagellida, Genome, Plastid, Phylogeny, Single-Cell Analysis, Transcriptome, Dinoflagellate evolution, noctilucoid, cryptic plastid, single-cell transcriptomics, Biochemistry and Cell Biology, Evolutionary Biology, Developmental Biology
Abstract

Dinoflagellates possess many cellular characteristics with unresolved evolutionary histories. These include nuclei with greatly expanded genomes and chromatin packaged using histone-like proteins and dinoflagellate-viral nucleoproteins instead of histones, highly reduced mitochondrial genomes with extensive RNA editing, a mix of photosynthetic and cryptic secondary plastids, and tertiary plastids. Resolving the evolutionary origin of these traits requires understanding their ancestral states and early intermediates. Several early-branching dinoflagellate lineages are good candidates for such reconstruction, however these cells tend to be delicate and environmentally sparse, complicating such analyses. Here, we employ transcriptome sequencing from manually isolated and microscopically documented cells to resolve the placement of two cells of one such genus, Abedinium, collected by remotely operated vehicle in deep waters off the coast of Monterey Bay, CA. One cell corresponds to the only described species, Abedinium dasypus, whereas the second cell is distinct and formally described as Abedinium folium, sp. nov. Abedinium has classically been assigned to the early-branching dinoflagellate subgroup Noctilucales, which is weakly supported by phylogenetic analyses of small subunit ribosomal RNA, the single characterized gene from any member of the order. However, an analysis based on 221 proteins from the transcriptome places Abedinium as a distinct lineage, separate from and basal to Noctilucales and the rest of the core dinoflagellates. The transcriptome also contains evidence of a cryptic plastid functioning in the biosynthesis of isoprenoids, iron-sulfur clusters, and heme, a mitochondrial genome with all three expected protein-coding genes (cob, cox1, and cox3), and the presence of some but not all dinoflagellate-specific chromatin packaging proteins.

Published
2020

13. Microbial predators form a new supergroup of eukaryotes

Author

Tikhonenkov, Denis V., Mikhailov, Kirill V., Gawryluk, Ryan M. R., Belyaev, Artem O., Mathur, Varsha, Karpov, Sergey A., Zagumyonnyi, Dmitry G., Borodina, Anastasia S., Prokina, Kristina I., Mylnikov, Alexander P., Aleoshin, Vladimir V., and Keeling, Patrick J.

Published
2022
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14. Genetic tool development in marine protists: emerging model organisms for experimental cell biology

Author

Faktorová, Drahomíra, Nisbet, R Ellen R, Fernández Robledo, José A, Casacuberta, Elena, Sudek, Lisa, Allen, Andrew E, Ares, Manuel, Aresté, Cristina, Balestreri, Cecilia, Barbrook, Adrian C, Beardslee, Patrick, Bender, Sara, Booth, David S, Bouget, François-Yves, Bowler, Chris, Breglia, Susana A, Brownlee, Colin, Burger, Gertraud, Cerutti, Heriberto, Cesaroni, Rachele, Chiurillo, Miguel A, Clemente, Thomas, Coles, Duncan B, Collier, Jackie L, Cooney, Elizabeth C, Coyne, Kathryn, Docampo, Roberto, Dupont, Christopher L, Edgcomb, Virginia, Einarsson, Elin, Elustondo, Pía A, Federici, Fernan, Freire-Beneitez, Veronica, Freyria, Nastasia J, Fukuda, Kodai, García, Paulo A, Girguis, Peter R, Gomaa, Fatma, Gornik, Sebastian G, Guo, Jian, Hampl, Vladimír, Hanawa, Yutaka, Haro-Contreras, Esteban R, Hehenberger, Elisabeth, Highfield, Andrea, Hirakawa, Yoshihisa, Hopes, Amanda, Howe, Christopher J, Hu, Ian, Ibañez, Jorge, Irwin, Nicholas AT, Ishii, Yuu, Janowicz, Natalia Ewa, Jones, Adam C, Kachale, Ambar, Fujimura-Kamada, Konomi, Kaur, Binnypreet, Kaye, Jonathan Z, Kazana, Eleanna, Keeling, Patrick J, King, Nicole, Klobutcher, Lawrence A, Lander, Noelia, Lassadi, Imen, Li, Zhuhong, Lin, Senjie, Lozano, Jean-Claude, Luan, Fulei, Maruyama, Shinichiro, Matute, Tamara, Miceli, Cristina, Minagawa, Jun, Moosburner, Mark, Najle, Sebastián R, Nanjappa, Deepak, Nimmo, Isabel C, Noble, Luke, Novák Vanclová, Anna MG, Nowacki, Mariusz, Nuñez, Isaac, Pain, Arnab, Piersanti, Angela, Pucciarelli, Sandra, Pyrih, Jan, Rest, Joshua S, Rius, Mariana, Robertson, Deborah, Ruaud, Albane, Ruiz-Trillo, Iñaki, Sigg, Monika A, Silver, Pamela A, Slamovits, Claudio H, Jason Smith, G, Sprecher, Brittany N, Stern, Rowena, Swart, Estienne C, Tsaousis, Anastasios D, Tsypin, Lev, Turkewitz, Aaron, and Turnšek, Jernej

Subjects
Genetics, Biotechnology, Life Below Water, Biodiversity, DNA, Ecosystem, Environment, Eukaryota, Green Fluorescent Proteins, Marine Biology, Models, Biological, Species Specificity, Transformation, Genetic, Biological Sciences, Technology, Medical and Health Sciences, Developmental Biology
Abstract

Diverse microbial ecosystems underpin life in the sea. Among these microbes are many unicellular eukaryotes that span the diversity of the eukaryotic tree of life. However, genetic tractability has been limited to a few species, which do not represent eukaryotic diversity or environmentally relevant taxa. Here, we report on the development of genetic tools in a range of protists primarily from marine environments. We present evidence for foreign DNA delivery and expression in 13 species never before transformed and for advancement of tools for eight other species, as well as potential reasons for why transformation of yet another 17 species tested was not achieved. Our resource in genetic manipulation will provide insights into the ancestral eukaryotic lifeforms, general eukaryote cell biology, protein diversification and the evolution of cellular pathways.

Published
2020

15. Publisher Correction: Genetic tool development in marine protists: emerging model organisms for experimental cell biology

Author

Faktorová, Drahomíra, Nisbet, R Ellen R, Fernández Robledo, José A, Casacuberta, Elena, Sudek, Lisa, Allen, Andrew E, Ares, Manuel, Aresté, Cristina, Balestreri, Cecilia, Barbrook, Adrian C, Beardslee, Patrick, Bender, Sara, Booth, David S, Bouget, François-Yves, Bowler, Chris, Breglia, Susana A, Brownlee, Colin, Burger, Gertraud, Cerutti, Heriberto, Cesaroni, Rachele, Chiurillo, Miguel A, Clemente, Thomas, Coles, Duncan B, Collier, Jackie L, Cooney, Elizabeth C, Coyne, Kathryn, Docampo, Roberto, Dupont, Christopher L, Edgcomb, Virginia, Einarsson, Elin, Elustondo, Pía A, Federici, Fernan, Freire-Beneitez, Veronica, Freyria, Nastasia J, Fukuda, Kodai, García, Paulo A, Girguis, Peter R, Gomaa, Fatma, Gornik, Sebastian G, Guo, Jian, Hampl, Vladimír, Hanawa, Yutaka, Haro-Contreras, Esteban R, Hehenberger, Elisabeth, Highfield, Andrea, Hirakawa, Yoshihisa, Hopes, Amanda, Howe, Christopher J, Hu, Ian, Ibañez, Jorge, Irwin, Nicholas AT, Ishii, Yuu, Janowicz, Natalia Ewa, Jones, Adam C, Kachale, Ambar, Fujimura-Kamada, Konomi, Kaur, Binnypreet, Kaye, Jonathan Z, Kazana, Eleanna, Keeling, Patrick J, King, Nicole, Klobutcher, Lawrence A, Lander, Noelia, Lassadi, Imen, Li, Zhuhong, Lin, Senjie, Lozano, Jean-Claude, Luan, Fulei, Maruyama, Shinichiro, Matute, Tamara, Miceli, Cristina, Minagawa, Jun, Moosburner, Mark, Najle, Sebastián R, Nanjappa, Deepak, Nimmo, Isabel C, Noble, Luke, Novák Vanclová, Anna MG, Nowacki, Mariusz, Nuñez, Isaac, Pain, Arnab, Piersanti, Angela, Pucciarelli, Sandra, Pyrih, Jan, Rest, Joshua S, Rius, Mariana, Robertson, Deborah, Ruaud, Albane, Ruiz-Trillo, Iñaki, Sigg, Monika A, Silver, Pamela A, Slamovits, Claudio H, Jason Smith, G, Sprecher, Brittany N, Stern, Rowena, Swart, Estienne C, Tsaousis, Anastasios D, Tsypin, Lev, Turkewitz, Aaron, and Turnšek, Jernej

Subjects
Biological Sciences, Technology, Medical and Health Sciences, Developmental Biology
Abstract

An amendment to this paper has been published and can be accessed via a link at the top of the paper.

Published
2020

20. A distinct lineage of giant viruses brings a rhodopsin photosystem to unicellular marine predators

Author

Needham, David M, Yoshizawa, Susumu, Hosaka, Toshiaki, Poirier, Camille, Choi, Chang Jae, Hehenberger, Elisabeth, Irwin, Nicholas AT, Wilken, Susanne, Yung, Cheuk-Man, Bachy, Charles, Kurihara, Rika, Nakajima, Yu, Kojima, Keiichi, Kimura-Someya, Tomomi, Leonard, Guy, Malmstrom, Rex R, Mende, Daniel R, Olson, Daniel K, Sudo, Yuki, Sudek, Sebastian, Richards, Thomas A, DeLong, Edward F, Keeling, Patrick J, Santoro, Alyson E, Shirouzu, Mikako, Iwasaki, Wataru, and Worden, Alexandra Z

Subjects
Microbiology, Biological Sciences, Ecology, Genetics, Infectious Diseases, Neurosciences, Infection, Life Below Water, Biological Evolution, Ecosystem, Eukaryota, Genome, Viral, Giant Viruses, Metagenomics, Oceans and Seas, Phycodnaviridae, Phylogeny, Protons, Rhodopsin, Seawater, Viral Proteins, giant viruses, viral evolution, marine carbon cycle, single-cell genomics, host-virus interactions, host–virus interactions
Abstract

Giant viruses are remarkable for their large genomes, often rivaling those of small bacteria, and for having genes thought exclusive to cellular life. Most isolated to date infect nonmarine protists, leaving their strategies and prevalence in marine environments largely unknown. Using eukaryotic single-cell metagenomics in the Pacific, we discovered a Mimiviridae lineage of giant viruses, which infects choanoflagellates, widespread protistan predators related to metazoans. The ChoanoVirus genomes are the largest yet from pelagic ecosystems, with 442 of 862 predicted proteins lacking known homologs. They are enriched in enzymes for modifying organic compounds, including degradation of chitin, an abundant polysaccharide in oceans, and they encode 3 divergent type-1 rhodopsins (VirR) with distinct evolutionary histories from those that capture sunlight in cellular organisms. One (VirRDTS) is similar to the only other putative rhodopsin from a virus (PgV) with a known host (a marine alga). Unlike the algal virus, ChoanoViruses encode the entire pigment biosynthesis pathway and cleavage enzyme for producing the required chromophore, retinal. We demonstrate that the rhodopsin shared by ChoanoViruses and PgV binds retinal and pumps protons. Moreover, our 1.65-Å resolved VirRDTS crystal structure and mutational analyses exposed differences from previously characterized type-1 rhodopsins, all of which come from cellular organisms. Multiple VirR types are present in metagenomes from across surface oceans, where they are correlated with and nearly as abundant as a canonical marker gene from Mimiviridae Our findings indicate that light-dependent energy transfer systems are likely common components of giant viruses of photosynthetic and phagotrophic unicellular marine eukaryotes.

Published
2019

31. Exact and approximate moment closures for non-Markovian network epidemics

Author

Pellis, Lorenzo, House, Thomas, and Keeling, Matt J.

Subjects
Quantitative Biology - Populations and Evolution, Mathematics - Probability, 92D30, 05C21
Abstract

Moment-closure techniques are commonly used to generate low-dimensional deterministic models to approximate the average dynamics of stochastic systems on networks. The quality of such closures is usually difficult to asses and the relationship between model assumptions and closure accuracy are often difficult, if not impossible, to quantify. Here we carefully examine some commonly used moment closures, in particular a new one based on the concept of maximum entropy, for approximating the spread of epidemics on networks by reconstructing the probability distributions over triplets based on those over pairs. We consider various models (SI, SIR, SEIR and Reed-Frost-type) under Markovian and non-Markovian assumption characterising the latent and infectious periods. We initially study two special networks, namely the open triplet and closed triangle, for which we can obtain analytical results. We then explore numerically the exactness of moment closures for a wide range of larger motifs, thus gaining understanding of the factors that introduce errors in the approximations, in particular the presence of a random duration of the infectious period and the presence of overlapping triangles in a network. We also derive a simpler and more intuitive proof than previously available concerning the known result that pair-based moment closure is exact for the Markovian SIR model on tree-like networks under pure initial conditions. We also extend such a result to all infectious models, Markovian and non-Markovian, in which susceptibles escape infection independently from each infected neighbour and for which infectives cannot regain susceptible status, provided the network is tree-like and initial conditions are pure. This works represent a valuable step in deepening understanding of the assumptions behind moment closure approximations and for putting them on a more rigorous mathematical footing., Comment: Main text (45 pages, 11 figures and 3 tables) + supplementary material (12 pages, 10 figures and 1 table). Accepted for publication in Journal of Theoretical Biology on 27th April 2015

Published
2015

33. Digital database for nasal prosthesis design with a 3D morphable face model approach.

Author

Jablonski, Rachael Y., Malhotra, Taran, Coward, Trevor J., Shaw, Daniel, Bojke, Chris, Pavitt, Sue H., Nattress, Brian R., and Keeling, Andrew J.

Abstract

Designing nasal prostheses can be challenging because of the unpaired nature of the facial feature, especially in patients lacking preoperative information. Various nose model databases have been developed as a helpful starting point for the computer-aided design of nasal prostheses, but these do not appear to be readily accessible. Therefore, an open-access digital database of nose models has been generated based on a 3-dimensional (3D) morphable face model approach. This article describes the generation of the database, highlights steps for designing a nasal prosthesis, and points readers to the database for future clinical application and research. [ABSTRACT FROM AUTHOR]

Published
2024
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35. The Nosoi commute: a spatial perspective on the rise of BSL-4 laboratories in cities

Author

Van Boeckel, Thomas P., Tildesley, Michael J., Linard, Catherine, Halloy, José, Keeling, Matt J., and Gilbert, Marius

Subjects
Quantitative Biology - Populations and Evolution
Abstract

Recent H5N1 influenza research has revived the debate on the storage and manipulation of potentially harmful pathogens. In the last two decades, new high biosafety (BSL-4) laboratories entered into operation, raising strong concerns from the public. The probability of an accidental release of a pathogen from a BSL-4 laboratory is extremely low, but the corresponding risk -- defined as the probability of occurrence multiplied by its impact -- could be significant depending on the pathogen specificities and the population potentially affected. A list of BSL-4 laboratories throughout the world, with their location and date of first activity, was established from publicly available sources. This database was used to estimate the total population living within a daily commuting distance of BSL-4 laboratories, and to quantify how this figure changed over time. We show that from 1990 to present, the population living within the commuting belt of BSL-4 laboratories increased by a factor of 4 to reach up to 1.8% of the world population, owing to an increase in the number of facilities and their installation in cities. Europe is currently hosting the largest population living in the direct vicinity of BSL-4 laboratories, while the recent building of new facilities in Asia suggests that an important increase of the population living close to BSL-4 laboratories will be observed in the next decades. We discuss the potential implications in term of global risk, and call for better pathogen-specific quantitative assessment of the risk of outbreaks resulting from the accidental release of potentially pandemic pathogens

Published
2013

46. Epidemic prediction and control in clustered populations

Author

House, Thomas and Keeling, Matt J

Subjects
Quantitative Biology - Populations and Evolution
Abstract

There has been much recent interest in modelling epidemics on networks, particularly in the presence of substantial clustering. Here, we develop pairwise methods to answer questions that are often addressed using epidemic models, in particular: on the basis of potential observations early in an outbreak, what can be predicted about the epidemic outcomes and the levels of intervention necessary to control the epidemic? We find that while some results are independent of the level of clustering (early growth predicts the level of `leaky' vaccine needed for control and peak time, while the basic reproductive ratio predicts the random vaccination threshold) the relationship between other quantities is very sensitive to clustering., Comment: 13 pages, 3 figures, to appear in the Journal of Theoretical Biology

Published
2010

47. Networks and the Epidemiology of Infectious Disease

Author

Danon, Leon, Ford, Ashley P., House, Thomas, Jewell, Chris P., Keeling, Matt J., Roberts, Gareth O., Ross, Joshua V., and Vernon, Matthew C.

Subjects
Physics - Physics and Society, Computer Science - Social and Information Networks, Quantitative Biology - Populations and Evolution
Abstract

The science of networks has revolutionised research into the dynamics of interacting elements. It could be argued that epidemiology in particular has embraced the potential of network theory more than any other discipline. Here we review the growing body of research concerning the spread of infectious diseases on networks, focusing on the interplay between network theory and epidemiology. The review is split into four main sections, which examine: the types of network relevant to epidemiology; the multitude of ways these networks can be characterised; the statistical methods that can be applied to infer the epidemiological parameters on a realised network; and finally simulation and analytical methods to determine epidemic dynamics on a given network. Given the breadth of areas covered and the ever-expanding number of publications, a comprehensive review of all work is impossible. Instead, we provide a personalised overview into the areas of network epidemiology that have seen the greatest progress in recent years or have the greatest potential to provide novel insights. As such, considerable importance is placed on analytical approaches and statistical methods which are both rapidly expanding fields. Throughout this review we restrict our attention to epidemiological issues., Comment: 51 pages, 3 figure, submitted

Published
2010
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48. The Marine Microbial Eukaryote Transcriptome Sequencing Project (MMETSP): illuminating the functional diversity of eukaryotic life in the oceans through transcriptome sequencing.

Author

Keeling, Patrick J, Burki, Fabien, Wilcox, Heather M, Allam, Bassem, Allen, Eric E, Amaral-Zettler, Linda A, Armbrust, E Virginia, Archibald, John M, Bharti, Arvind K, Bell, Callum J, Beszteri, Bank, Bidle, Kay D, Cameron, Connor T, Campbell, Lisa, Caron, David A, Cattolico, Rose Ann, Collier, Jackie L, Coyne, Kathryn, Davy, Simon K, Deschamps, Phillipe, Dyhrman, Sonya T, Edvardsen, Bente, Gates, Ruth D, Gobler, Christopher J, Greenwood, Spencer J, Guida, Stephanie M, Jacobi, Jennifer L, Jakobsen, Kjetill S, James, Erick R, Jenkins, Bethany, John, Uwe, Johnson, Matthew D, Juhl, Andrew R, Kamp, Anja, Katz, Laura A, Kiene, Ronald, Kudryavtsev, Alexander, Leander, Brian S, Lin, Senjie, Lovejoy, Connie, Lynn, Denis, Marchetti, Adrian, McManus, George, Nedelcu, Aurora M, Menden-Deuer, Susanne, Miceli, Cristina, Mock, Thomas, Montresor, Marina, Moran, Mary Ann, Murray, Shauna, Nadathur, Govind, Nagai, Satoshi, Ngam, Peter B, Palenik, Brian, Pawlowski, Jan, Petroni, Giulio, Piganeau, Gwenael, Posewitz, Matthew C, Rengefors, Karin, Romano, Giovanna, Rumpho, Mary E, Rynearson, Tatiana, Schilling, Kelly B, Schroeder, Declan C, Simpson, Alastair GB, Slamovits, Claudio H, Smith, David R, Smith, G Jason, Smith, Sarah R, Sosik, Heidi M, Stief, Peter, Theriot, Edward, Twary, Scott N, Umale, Pooja E, Vaulot, Daniel, Wawrik, Boris, Wheeler, Glen L, Wilson, William H, Xu, Yan, Zingone, Adriana, and Worden, Alexandra Z

Subjects
Sequence Analysis, Environmental Microbiology, Biodiversity, Molecular Sequence Data, Databases, Factual, Oceans and Seas, Eukaryota, Transcriptome, Databases, Factual, Developmental Biology, Biological Sciences, Medical and Health Sciences, Agricultural and Veterinary Sciences
Published
2014

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