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3. Viruses interact with hosts that span distantly related microbial domains in dense hydrothermal mats

Author

Hwang, Yunha, Roux, Simon, Coclet, Clément, Krause, Sebastian JE, and Girguis, Peter R

Subjects
Microbiology, Biological Sciences, Emerging Infectious Diseases, Genetics, Infectious Diseases, 2.2 Factors relating to the physical environment, Aetiology, Infection, Bacteria, Ecosystem, Viruses, DNA, Microbial Interactions, Medical Microbiology
Abstract

Many microbes in nature reside in dense, metabolically interdependent communities. We investigated the nature and extent of microbe-virus interactions in relation to microbial density and syntrophy by examining microbe-virus interactions in a biomass dense, deep-sea hydrothermal mat. Using metagenomic sequencing, we find numerous instances where phylogenetically distant (up to domain level) microbes encode CRISPR-based immunity against the same viruses in the mat. Evidence of viral interactions with hosts cross-cutting microbial domains is particularly striking between known syntrophic partners, for example those engaged in anaerobic methanotrophy. These patterns are corroborated by proximity-ligation-based (Hi-C) inference. Surveys of public datasets reveal additional viruses interacting with hosts across domains in diverse ecosystems known to harbour syntrophic biofilms. We propose that the entry of viral particles and/or DNA to non-primary host cells may be a common phenomenon in densely populated ecosystems, with eco-evolutionary implications for syntrophic microbes and CRISPR-mediated inter-population augmentation of resilience against viruses.

Published
2023

5. Carbonate-hosted microbial communities are prolific and pervasive methane oxidizers at geologically diverse marine methane seep sites

Author

Marlow, Jeffrey J, Hoer, Daniel, Jungbluth, Sean P, Reynard, Linda M, Gartman, Amy, Chavez, Marko S, El-Naggar, Mohamed Y, Tuross, Noreen, Orphan, Victoria J, and Girguis, Peter R

Subjects
Earth Sciences, Biological Sciences, Geology, Life Below Water, Carbonates, Geography, Geological Phenomena, Kinetics, Methane, Microbiota, Oxidation-Reduction, RNA, Ribosomal, 16S, Seawater, methane oxidation, metabolic rates, endolith, methane seep
Abstract

At marine methane seeps, vast quantities of methane move through the shallow subseafloor, where it is largely consumed by microbial communities. This process plays an important role in global methane dynamics, but we have yet to identify all of the methane sinks in the deep sea. Here, we conducted a continental-scale survey of seven geologically diverse seafloor seeps and found that carbonate rocks from all sites host methane-oxidizing microbial communities with substantial methanotrophic potential. In laboratory-based mesocosm incubations, chimney-like carbonates from the newly described Point Dume seep off the coast of Southern California exhibited the highest rates of anaerobic methane oxidation measured to date. After a thorough analysis of physicochemical, electrical, and biological factors, we attribute this substantial metabolic activity largely to higher cell density, mineral composition, kinetic parameters including an elevated Vmax, and the presence of specific microbial lineages. Our data also suggest that other features, such as electrical conductance, rock particle size, and microbial community alpha diversity, may influence a sample's methanotrophic potential, but these factors did not demonstrate clear patterns with respect to methane oxidation rates. Based on the apparent pervasiveness within seep carbonates of microbial communities capable of performing anaerobic oxidation of methane, as well as the frequent occurrence of carbonates at seeps, we suggest that rock-hosted methanotrophy may be an important contributor to marine methane consumption.

Published
2021

6. OCEAN SYSTEM SCIENCE TO INFORM THE EXPLORATION OF OCEAN WORLDS

Author

German, Christopher R., Blackman, Donna K., Fisher, Andrew T., Girguis, Peter R., Hand, Kevin P., Hoehler, Tori M., Huber, Julie A., Marshall, John C., Pietro, Kathryn R., Seewald, Jeffrey S., Shock, Everett L., Sotin, Christophe, Thurnherr, Andreas M., and Toner, Brandy M.

Published
2022

7. 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

8. 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

9. 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

10. Vortex fluidics-mediated DNA rescue from formalin-fixed museum specimens.

Author

Totoiu, Christian A, Phillips, Jessica M, Reese, Aspen T, Majumdar, Sudipta, Girguis, Peter R, Raston, Colin L, and Weiss, Gregory A

Subjects
Animals, Nephropidae, Formaldehyde, DNA, Tissue Fixation, Polymerase Chain Reaction, Base Sequence, Museums, Hydrodynamics, General Science & Technology
Abstract

DNA from formalin-preserved tissue could unlock a vast repository of genetic information stored in museums worldwide. However, formaldehyde crosslinks proteins and DNA, and prevents ready amplification and DNA sequencing. Formaldehyde acylation also fragments the DNA. Treatment with proteinase K proteolyzes crosslinked proteins to rescue the DNA, though the process is quite slow. To reduce processing time and improve rescue efficiency, we applied the mechanical energy of a vortex fluidic device (VFD) to drive the catalytic activity of proteinase K and recover DNA from American lobster tissue (Homarus americanus) fixed in 3.7% formalin for >1-year. A scan of VFD rotational speeds identified the optimal rotational speed for recovery of PCR-amplifiable DNA and while 500+ base pairs were sequenced, shorter read lengths were more consistently obtained. This VFD-based method also effectively recovered DNA from formalin-preserved samples. The results provide a roadmap for exploring DNA from millions of historical and even extinct species.

Published
2020

15. Telepresence is a potentially transformative tool for field science

Author

Marlow, Jeffrey, Borrelli, Chiara, Jungbluth, Sean P, Hoffman, Colleen, Marlow, Jennifer, Girguis, Peter R, Dekas, Anne, Skarke, Adam, Blackman, Donna, Fornari, Dan, Soule, Adam, Van Dover, Cindy, Bagge, Laura, Barco, Roman, Boulahanais, Bridgit, Bowman, Kaitlin, Brugler, Mercer, Bush, Stephanie, Djurhuus, Anni, Fernandez, Julianne, Fulweiler, Robinson, Jungbluth, Sean, Kinsey, Joanna, Kocot, Kevin, McVeigh, Doreen, Navarro, Michael, Netburn, Amanda, Pasulka, Alexis, Twing, Katrina, Wagner, Amy, and Zambon, Joe

Subjects
AT-36 Team
Published
2017

16. Sulfur cycling likely obscures dynamic biologically‐driven iron redox cycling in contemporary methane seep environments.

Author

Baker, Isabel R. and Girguis, Peter R.

Subjects
*COLD seeps, *PYRITES, *IRON sulfides, *IRON, *IRON oxidation, *SULFUR cycle, *CYCLING competitions, *BATCH reactors
Abstract

Deep‐sea methane seeps are amongst the most biologically productive environments on Earth and are often characterised by stable, low oxygen concentrations and microbial communities that couple the anaerobic oxidation of methane to sulfate reduction or iron reduction in the underlying sediment. At these sites, ferrous iron (Fe2+) can be produced by organoclastic iron reduction, methanotrophic‐coupled iron reduction, or through the abiotic reduction by sulfide produced by the abundant sulfate‐reducing bacteria at these sites. The prevalence of Fe2+in the anoxic sediments, as well as the availability of oxygen in the overlying water, suggests that seeps could also harbour communities of iron‐oxidising microbes. However, it is unclear to what extent Fe2+ remains bioavailable and in solution given that the abiotic reaction between sulfide and ferrous iron is often assumed to scavenge all ferrous iron as insoluble iron sulfides and pyrite. Accordingly, we searched the sea floor at methane seeps along the Cascadia Margin for microaerobic, neutrophilic iron‐oxidising bacteria, operating under the reasoning that if iron‐oxidising bacteria could be isolated from these environments, it could indicate that porewater Fe2+ can persist is long enough for biology to outcompete pyritisation. We found that the presence of sulfate in our enrichment media muted any obvious microbially‐driven iron oxidation with most iron being precipitated as iron sulfides. Transfer of enrichment cultures to sulfate‐depleted media led to dynamic iron redox cycling relative to abiotic controls and sulfate‐containing cultures, and demonstrated the capacity for biogenic iron (oxyhydr)oxides from a methane seep‐derived community. 16S rRNA analyses revealed that removing sulfate drastically reduced the diversity of enrichment cultures and caused a general shift from a Gammaproteobacteria‐domainated ecosystem to one dominated by Rhodobacteraceae (Alphaproteobacteria). Our data suggest that, in most cases, sulfur cycling may restrict the biological "ferrous wheel" in contemporary environments through a combination of the sulfur‐adapted sediment‐dwelling ecosystems and the abiotic reactions they influence. [ABSTRACT FROM AUTHOR]

Published
2024
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22. Oxygen, ecology, and the Cambrian radiation of animals

Author

Sperling, Erik A, Frieder, Christina A, Raman, Akkur V, Girguis, Peter R, Levin, Lisa A, and Knoll, Andrew H

Subjects
Analysis of Variance, Animals, Biodiversity, Biological Evolution, Feeding Behavior, Food Chain, Fossils, Oceans and Seas, Oxygen, Paleontology, evolution, hypoxia, Ediacaran, Metazoa
Abstract

The Proterozoic-Cambrian transition records the appearance of essentially all animal body plans (phyla), yet to date no single hypothesis adequately explains both the timing of the event and the evident increase in diversity and disparity. Ecological triggers focused on escalatory predator-prey "arms races" can explain the evolutionary pattern but not its timing, whereas environmental triggers, particularly ocean/atmosphere oxygenation, do the reverse. Using modern oxygen minimum zones as an analog for Proterozoic oceans, we explore the effect of low oxygen levels on the feeding ecology of polychaetes, the dominant macrofaunal animals in deep-sea sediments. Here we show that low oxygen is clearly linked to low proportions of carnivores in a community and low diversity of carnivorous taxa, whereas higher oxygen levels support more complex food webs. The recognition of a physiological control on carnivory therefore links environmental triggers and ecological drivers, providing an integrated explanation for both the pattern and timing of Cambrian animal radiation.

Published
2013

34. 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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40. Low-Cost, Deep-Sea Imaging and Analysis Tools for Deep-Sea Exploration: A Collaborative Design Study

Author

Bell, Katherine L. C., primary, Chow, Jennifer Szlosek, additional, Hope, Alexis, additional, Quinzin, Maud C., additional, Cantner, Kat A., additional, Amon, Diva J., additional, Cramp, Jessica E., additional, Rotjan, Randi D., additional, Kamalu, Lehua, additional, de Vos, Asha, additional, Talma, Sheena, additional, Buglass, Salome, additional, Wade, Veta, additional, Filander, Zoleka, additional, Noyes, Kaitlin, additional, Lynch, Miriam, additional, Knight, Ashley, additional, Lourenço, Nuno, additional, Girguis, Peter R., additional, de Sousa, João Borges, additional, Blake, Chris, additional, Kennedy, Brian R. C., additional, Noyes, Timothy J., additional, and McClain, Craig R., additional

Published
2022
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