Viral Communities of Shark Bay Modern Stromatolites

White, Richard Allen; Wong, Hon L.; Ruvindy, Rendy; Neilan, Brett A.; Burns, Brendan P.

doi:10.3389/fmicb.2018.01223

Viral Communities of Shark Bay Modern Stromatolites

Journal Article · Wed Jun 13 00:00:00 EDT 2018 · Frontiers in Microbiology

DOI:https://doi.org/10.3389/fmicb.2018.01223· OSTI ID:1728612

White, Richard Allen ^[1]; Wong, Hon L. ^[2]; Ruvindy, Rendy ^[2]; Neilan, Brett A. ^[2]; Burns, Brendan P. ^[2]

Washington State Univ., Pullman, WA (United States); Univ. of New South Wales, Sydney, NSW (Australia); RAW Molecular Systems (RMS) LLC, Spokane, WA (United States)
Univ. of New South Wales, Sydney, NSW (Australia)

Single stranded DNA viruses have been previously shown to populate the oceans on a global scale, and are endemic in microbialites of both marine and freshwater systems. We undertook for the first time direct viral metagenomic shotgun sequencing to explore the diversity of viruses in the modern stromatolites of Shark Bay Australia. The data indicate that Shark Bay marine stromatolites have similar diversity of ssDNA viruses to that of Highbourne Cay, Bahamas. ssDNA viruses in cluster uniquely in Shark Bay and Highbourne Cay, potentially due to enrichment by phi29-mediated amplification bias. Further, pyrosequencing data was assembled from the Shark Bay systems into two putative viral genomes that are related to Genomoviridae family of ssDNA viruses. In addition, the cellular fraction was shown to be enriched for antiviral defense genes including CRISPR-Cas, BREX (bacteriophage exclusion), and DISARM (defense island system associated with restriction-modification), a potentially novel finding for these systems. This is the first evidence for viruses in the Shark Bay stromatolites, and these viruses may play key roles in modulating microbial diversity as well as potentially impacting ecosystem function through infection and the recycling of key nutrients.

View Accepted Manuscript (DOE)

Research Organization:: Pacific Northwest National Laboratory (PNNL), Richland, WA (United States)

Sponsoring Organization:: Australian Research Council (ARC); USDOE

Grant/Contract Number:: AC05-76RL01830

OSTI ID:: 1728612

Report Number(s):: PNNL-SA--123161

Journal Information:: Frontiers in Microbiology, Journal Name: Frontiers in Microbiology Vol. 9; ISSN 1664-302X

Publisher:: Frontiers Research FoundationCopyright Statement

Country of Publication:: United States

Language:: English

References (70)

Application of molecular techniques to addressing the role of P as a key effector in marine ecosystems Scanlan, D. J.; Wilson, W. H. Molecular Ecology of Aquatic Communities https://doi.org/10.1007/978-94-011-4201-4_12	book	January 1999
Low phosphorus sediments in a hypersaline marine bay Atkinson, M. J. Estuarine, Coastal and Shelf Science, Vol. 24, Issue 3 https://doi.org/10.1016/0272-7714(87)90054-0	journal	March 1987
BlastKOALA and GhostKOALA: KEGG Tools for Functional Characterization of Genome and Metagenome Sequences Kanehisa, Minoru; Sato, Yoko; Morishima, Kanae Journal of Molecular Biology, Vol. 428, Issue 4 https://doi.org/10.1016/j.jmb.2015.11.006	journal	February 2016
Characterisation of a diverse range of circular replication-associated protein encoding DNA viruses recovered from a sewage treatment oxidation pond Kraberger, Simona; Argüello-Astorga, Gerardo R.; Greenfield, Laurence G. Infection, Genetics and Evolution, Vol. 31 https://doi.org/10.1016/j.meegid.2015.01.001	journal	April 2015
Geological setting of Earth's oldest fossils in the ca. 3.5Ga Dresser Formation, Pilbara Craton, Western Australia Vankranendonk, M.; Philippot, P.; Lepot, K. Precambrian Research, Vol. 167, Issue 1-2 https://doi.org/10.1016/j.precamres.2008.07.003	journal	November 2008
Microbial lithification in marine stromatolites and hypersaline mats Dupraz, Christophe; Visscher, Pieter T. Trends in Microbiology, Vol. 13, Issue 9 https://doi.org/10.1016/j.tim.2005.07.008	journal	September 2005
Phosphorus limitation of net production in a confined aquatic ecosystem Smith, S. V.; Atkinson, M. J. Nature, Vol. 307, Issue 5952 https://doi.org/10.1038/307626a0	journal	February 1984
Determining the specific microbial populations and their spatial distribution within the stromatolite ecosystem of Shark Bay Goh, Falicia; Allen, Michelle A.; Leuko, Stefan The ISME Journal, Vol. 3, Issue 4 https://doi.org/10.1038/ismej.2008.114	journal	December 2008
Active eukaryotes in microbialites from Highborne Cay, Bahamas, and Hamelin Pool (Shark Bay), Australia Edgcomb, Virginia P.; Bernhard, Joan M.; Summons, Roger E. The ISME Journal, Vol. 8, Issue 2 https://doi.org/10.1038/ismej.2013.130	journal	August 2013
Diversity of environmental single-stranded DNA phages revealed by PCR amplification of the partial major capsid protein Hopkins, Max; Kailasan, Shweta; Cohen, Allison The ISME Journal, Vol. 8, Issue 10 https://doi.org/10.1038/ismej.2014.43	journal	April 2014
Genome sequencing in microfabricated high-density picolitre reactors Margulies, Marcel; Egholm, Michael; Altman, William E. Nature, Vol. 437, Issue 7057, p. 376-380 https://doi.org/10.1038/nature03959	journal	July 2005
Viruses in the sea Suttle, Curtis A. Nature, Vol. 437, Issue 7057 https://doi.org/10.1038/nature04160	journal	September 2005
Biodiversity and biogeography of phages in modern stromatolites and thrombolites Desnues, Christelle; Rodriguez-Brito, Beltran; Rayhawk, Steve Nature, Vol. 452, Issue 7185 https://doi.org/10.1038/nature06735	journal	March 2008
Tracing the steps of Zika virus Hofer, Ursula Nature Reviews Microbiology, Vol. 14, Issue 7 https://doi.org/10.1038/nrmicro.2016.80	journal	May 2016
Marine viruses — major players in the global ecosystem Suttle, Curtis A. Nature Reviews Microbiology, Vol. 5, Issue 10 https://doi.org/10.1038/nrmicro1750	journal	October 2007
Rhizosphere bacteriome structure and functions Ling, Ning; Wang, Tingting; Kuzyakov, Yakov Nature Communications, Vol. 13, Issue 1 https://doi.org/10.1038/s41467-022-28448-9	journal	February 2022
DISARM is a widespread bacterial defence system with broad anti-phage activities Ofir, Gal; Melamed, Sarah; Sberro, Hila Nature Microbiology, Vol. 3, Issue 1 https://doi.org/10.1038/s41564-017-0051-0	journal	October 2017
Dyeing to connect Johnson, Cydney N.; Duerkop, Breck A. Nature Microbiology, Vol. 4, Issue 12 https://doi.org/10.1038/s41564-019-0616-1	journal	November 2019
Integrating cultivation and metagenomics for a multi-kingdom view of skin microbiome diversity and functions Saheb Kashaf, Sara; Proctor, Diana M.; Deming, Clay Nature Microbiology, Vol. 7, Issue 1 https://doi.org/10.1038/s41564-021-01011-w	journal	December 2021
A marine inducible prophage vB_CibM-P1 isolated from the aerobic anoxygenic phototrophic bacterium Citromicrobium bathyomarinum JL354 Zheng, Qiang; Zhang, Rui; Xu, Yongle Scientific Reports, Vol. 4, Issue 1 https://doi.org/10.1038/srep07118	journal	November 2014
Niche differentiation of bacterial communities at a millimeter scale in Shark Bay microbial mats Wong, Hon Lun; Smith, Daniela-Lee; Visscher, Pieter T. Scientific Reports, Vol. 5, Issue 1 https://doi.org/10.1038/srep15607	journal	October 2015
Dynamics of archaea at fine spatial scales in Shark Bay mat microbiomes Wong, Hon Lun; Visscher, Pieter T.; White III, Richard Allen Scientific Reports, Vol. 7, Issue 1 https://doi.org/10.1038/srep46160	journal	April 2017
Phage auxiliary metabolic genes and the redirection of cyanobacterial host carbon metabolism Thompson, L. R.; Zeng, Q.; Kelly, L. Proceedings of the National Academy of Sciences, Vol. 108, Issue 39 https://doi.org/10.1073/pnas.1102164108	journal	August 2011
Ray: Simultaneous Assembly of Reads from a Mix of High-Throughput Sequencing Technologies Boisvert, Sébastien; Laviolette, François; Corbeil, Jacques Journal of Computational Biology, Vol. 17, Issue 11 https://doi.org/10.1089/cmb.2009.0238	journal	November 2010
Quality control and preprocessing of metagenomic datasets Schmieder, R.; Edwards, R. Bioinformatics, Vol. 27, Issue 6 https://doi.org/10.1093/bioinformatics/btr026	journal	January 2011
Metavir: a web server dedicated to virome analysis Roux, Simon; Faubladier, Michaël; Mahul, Antoine Bioinformatics, Vol. 27, Issue 21 https://doi.org/10.1093/bioinformatics/btr519	journal	September 2011
InterProScan 5: genome-scale protein function classification Jones, P.; Binns, D.; Chang, H. -Y. Bioinformatics, Vol. 30, Issue 9 https://doi.org/10.1093/bioinformatics/btu031	journal	January 2014
Single-stranded DNA phages: from early molecular biology tools to recent revolutions in environmental microbiology Székely, Anna J.; Breitbart, Mya FEMS Microbiology Letters, Vol. 363, Issue 6 https://doi.org/10.1093/femsle/fnw027	journal	February 2016
MUSCLE: multiple sequence alignment with high accuracy and high throughput Edgar, R. C. Nucleic Acids Research, Vol. 32, Issue 5, p. 1792-1797 https://doi.org/10.1093/nar/gkh340	journal	March 2004
Diverse circovirus-like genome architectures revealed by environmental metagenomics Rosario, Karyna; Duffy, Siobain; Breitbart, Mya Journal of General Virology, Vol. 90, Issue 10 https://doi.org/10.1099/vir.0.012955-0	journal	October 2009
Alkaline phosphatases in microbialites and bacterioplankton from Alchichica soda lake, Mexico Valdespino-Castillo, Patricia M.; Alcántara-Hernández, Rocio J.; Alcocer, Javier FEMS Microbiology Ecology https://doi.org/10.1111/1574-6941.12411	journal	October 2014
Microbial diversity of extant stromatolites in the hypersaline marine environment of Shark Bay, Australia Burns, Brendan P.; Goh, Falicia; Allen, Michelle Environmental Microbiology, Vol. 6, Issue 10 https://doi.org/10.1111/j.1462-2920.2004.00651.x	journal	October 2004
Metagenomic analysis of viruses in reclaimed water Rosario, Karyna; Nilsson, Christina; Lim, Yan Wei Environmental Microbiology, Vol. 11, Issue 11 https://doi.org/10.1111/j.1462-2920.2009.01964.x	journal	November 2009
Bacterial, archaeal and eukaryotic diversity of smooth and pustular microbial mat communities in the hypersaline lagoon of Shark Bay Allen, M. A.; Goh, F.; Burns, B. P. Geobiology, Vol. 7, Issue 1 https://doi.org/10.1111/j.1472-4669.2008.00187.x	journal	January 2009
Amplification Methods Bias Metagenomic Libraries of Uncultured Single-Stranded and Double-Stranded DNA Viruses Kim, Kyoung-Ho; Bae, Jin-Woo Applied and Environmental Microbiology, Vol. 77, Issue 21 https://doi.org/10.1128/aem.00289-11	journal	September 2011
Development of phoH as a Novel Signature Gene for Assessing Marine Phage Diversity Goldsmith, Dawn B.; Crosti, Giuseppe; Dwivedi, Bhakti Applied and Environmental Microbiology, Vol. 77, Issue 21 https://doi.org/10.1128/aem.05531-11	journal	September 2011
Prodigal: prokaryotic gene recognition and translation initiation site identification Hyatt, Doug; Chen, Gwo-Liang; LoCascio, Philip F. BMC Bioinformatics, Vol. 11, Issue 1 https://doi.org/10.1186/1471-2105-11-119	journal	March 2010
Metavir 2: new tools for viral metagenome comparison and assembled virome analysis Roux, Simon; Tournayre, Jeremy; Mahul, Antoine BMC Bioinformatics, Vol. 15, Issue 1 https://doi.org/10.1186/1471-2105-15-76	journal	January 2014
The metagenomics RAST server – a public resource for the automatic phylogenetic and functional analysis of metagenomes Meyer, F.; Paarmann, D.; D'Souza, M. BMC Bioinformatics, Vol. 9, Issue 1 https://doi.org/10.1186/1471-2105-9-386	journal	September 2008
On the alleged origin of geminiviruses from extrachromosomal DNAs of phytoplasmas Saccardo, Federica; Cettul, Emanuele; Palmano, Sabrina BMC Evolutionary Biology, Vol. 11, Issue 1 https://doi.org/10.1186/1471-2148-11-185	journal	June 2011
Ray Meta: scalable de novo metagenome assembly and profiling Boisvert, Sébastien; Raymond, Frédéric; Godzaridis, Élénie Genome Biology, Vol. 13, Issue 12 https://doi.org/10.1186/gb-2012-13-12-r122	journal	January 2012
The Marine Viromes of Four Oceanic Regions Angly, Florent E.; Felts, Ben; Breitbart, Mya PLoS Biology, Vol. 4, Issue 11 https://doi.org/10.1371/journal.pbio.0040368	journal	November 2006
Microviridae Goes Temperate: Microvirus-Related Proviruses Reside in the Genomes of Bacteroidetes Krupovic, Mart; Forterre, Patrick PLoS ONE, Vol. 6, Issue 5 https://doi.org/10.1371/journal.pone.0019893	journal	May 2011
BREX is a novel phage resistance system widespread in microbial genomes Goldfarb, Tamara; Sberro, Hila; Weinstock, Eyal The EMBO Journal, Vol. 34, Issue 2 https://doi.org/10.15252/embj.201489455	journal	December 2014
Incorporation of viruses into the budget of microbial C-transfer A first approach Bratbak, G.; Heldal, M.; Thingstad, Tf Marine Ecology Progress Series, Vol. 83 https://doi.org/10.3354/meps083273	journal	January 1992
Genomic characteristics and environmental distributions of the uncultivated Far-T4 phages Roux, Simon; Enault, François; Ravet, Viviane Frontiers in Microbiology, Vol. 6 https://doi.org/10.3389/fmicb.2015.00199	journal	March 2015
Metagenomic analysis reveals that modern microbialites and polar microbial mats have similar taxonomic and functional potential White, Richard Allen; Power, Ian M.; Dipple, Gregory M. Frontiers in Microbiology, Vol. 6 https://doi.org/10.3389/fmicb.2015.00966	journal	September 2015
Towards quantitative viromics for both double-stranded and single-stranded DNA viruses Roux, Simon; Solonenko, Natalie E.; Dang, Vinh T. PeerJ, Vol. 4 https://doi.org/10.7717/peerj.2777	journal	January 2016
Genomoviridae: a new family of widespread single-stranded DNA viruses Krupovic, Mart; Ghabrial, Said A.; Jiang, Daohong Archives of Virology, Vol. 161, Issue 9 https://doi.org/10.1007/s00705-016-2943-3	journal	June 2016
Processes of carbonate precipitation in modern microbial mats Dupraz, Christophe; Reid, R. Pamela; Braissant, Olivier Earth-Science Reviews, Vol. 96, Issue 3 https://doi.org/10.1016/j.earscirev.2008.10.005	journal	October 2009
Here a virus, there a virus, everywhere the same virus? Breitbart, Mya; Rohwer, Forest Trends in Microbiology, Vol. 13, Issue 6 https://doi.org/10.1016/j.tim.2005.04.003	journal	June 2005
Unravelling core microbial metabolisms in the hypersaline microbial mats of Shark Bay using high-throughput metagenomics Ruvindy, Rendy; White III, Richard Allen; Neilan, Brett Anthony The ISME Journal, Vol. 10, Issue 1 https://doi.org/10.1038/ismej.2015.87	journal	May 2015
Viruses in the faecal microbiota of monozygotic twins and their mothers Reyes, Alejandro; Haynes, Matthew; Hanson, Nicole Nature, Vol. 466, Issue 7304 https://doi.org/10.1038/nature09199	journal	July 2010
Uncovering Earth’s virome Paez-Espino, David; Eloe-Fadrosh, Emiley A.; Pavlopoulos, Georgios A. Nature, Vol. 536, Issue 7617 https://doi.org/10.1038/nature19094	journal	August 2016
Laboratory procedures to generate viral metagenomes Thurber, Rebecca V.; Haynes, Matthew; Breitbart, Mya Nature Protocols, Vol. 4, Issue 4 https://doi.org/10.1038/nprot.2009.10	journal	March 2009
The elemental composition of virus particles: implications for marine biogeochemical cycles Jover, Luis F.; Effler, T. Chad; Buchan, Alison Nature Reviews Microbiology, Vol. 12, Issue 7 https://doi.org/10.1038/nrmicro3289	journal	June 2014
New multi-scale perspectives on the stromatolites of Shark Bay, Western Australia Suosaari, E. P.; Reid, R. P.; Playford, P. E. Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep20557	journal	February 2016
Unipro UGENE: a unified bioinformatics toolkit Okonechnikov, Konstantin; Golosova, Olga; Fursov, Mikhail Bioinformatics, Vol. 28, Issue 8 https://doi.org/10.1093/bioinformatics/bts091	journal	February 2012
UFBoot2: Improving the Ultrafast Bootstrap Approximation Hoang, Diep Thi; Chernomor, Olga; von Haeseler, Arndt Molecular Biology and Evolution, Vol. 35, Issue 2 https://doi.org/10.1093/molbev/msx281	journal	October 2017
Interactive tree of life (iTOL) v3: an online tool for the display and annotation of phylogenetic and other trees Letunic, Ivica; Bork, Peer Nucleic Acids Research, Vol. 44, Issue W1 https://doi.org/10.1093/nar/gkw290	journal	April 2016
Viral ecology comes of age: Crystal ball Sullivan, Matthew B.; Weitz, Joshua S.; Wilhelm, Steven Environmental Microbiology Reports, Vol. 9, Issue 1 https://doi.org/10.1111/1758-2229.12504	journal	February 2017
CRISPR/Cas, the Immune System of Bacteria and Archaea Horvath, Philippe; Barrangou, Rodolphe Science, Vol. 327, Issue 5962 https://doi.org/10.1126/science.1179555	journal	January 2010
Amplification Methods Bias Metagenomic Libraries of Uncultured Single-Stranded and Double-Stranded DNA Viruses Kim, Kyoung-Ho; Bae, Jin-Woo Applied and Environmental Microbiology, Vol. 77, Issue 21 https://doi.org/10.1128/AEM.00289-11	journal	September 2011
Development of phoH as a Novel Signature Gene for Assessing Marine Phage Diversity Goldsmith, Dawn B.; Crosti, Giuseppe; Dwivedi, Bhakti Applied and Environmental Microbiology, Vol. 77, Issue 21 https://doi.org/10.1128/AEM.05531-11	journal	September 2011
Moleculo Long-Read Sequencing Facilitates Assembly and Genomic Binning from Complex Soil Metagenomes White, Richard Allen; Bottos, Eric M.; Roy Chowdhury, Taniya mSystems, Vol. 1, Issue 3 https://doi.org/10.1128/mSystems.00045-16	journal	June 2016
TagCleaner: Identification and removal of tag sequences from genomic and metagenomic datasets Schmieder, Robert; Lim, Yan Wei; Rohwer, Forest BMC Bioinformatics, Vol. 11, Issue 1 https://doi.org/10.1186/1471-2105-11-341	journal	June 2010
Single-cell transcriptomics using spliced leader PCR: Evidence for multiple losses of photosynthesis in polykrikoid dinoflagellates Gavelis, Gregory S.; White, Richard A.; Suttle, Curtis A. BMC Genomics, Vol. 16, Issue 1 https://doi.org/10.1186/s12864-015-1636-8	journal	July 2015
Metagenomic Analysis Suggests Modern Freshwater Microbialites Harbor a Distinct Core Microbial Community White, Richard Allen; Chan, Amy M.; Gavelis, Gregory S. Frontiers in Microbiology, Vol. 6 https://doi.org/10.3389/fmicb.2015.01531	journal	January 2016
Release and bioavailability of C, N, P Se, and Fe following viral lysis of a marine chrysophyte Gobler, Christopher J.; Hutchins, David A.; Fisher, Nicholas S. Limnology and Oceanography, Vol. 42, Issue 7 https://doi.org/10.4319/lo.1997.42.7.1492	journal	November 1997
Benchmarking viromics: an in silico evaluation of metagenome-enabled estimates of viral community composition and diversity Roux, Simon; Emerson, Joanne B.; Eloe-Fadrosh, Emiley A. PeerJ, Vol. 5 https://doi.org/10.7717/peerj.3817	journal	January 2017

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