DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Viruses interact with hosts that span distantly related microbial domains in dense hydrothermal mats

Abstract

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.

Authors:
ORCiD logo; ; ORCiD logo; ; ORCiD logo
Publication Date:
Research Org.:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States); USDOE Joint Genome Institute (JGI), Berkeley, CA (United States)
Sponsoring Org.:
USDOE; USDOE Office of Science (SC), Basic Energy Sciences (BES). Scientific User Facilities (SUF); Gordon and Betty Moore Foundation; National Science Foundation (NSF); National Aeronautics and Space Administration (NASA)
OSTI Identifier:
1968630
Alternate Identifier(s):
OSTI ID: 2234130
Grant/Contract Number:  
AC02-05CH11231; 9208; OCE-1635365; 80NSSC18K1140; 80NSSC19K1427
Resource Type:
Published Article
Journal Name:
Nature Microbiology
Additional Journal Information:
Journal Name: Nature Microbiology Journal Volume: 8 Journal Issue: 5; Journal ID: ISSN 2058-5276
Publisher:
Nature Publishing Group
Country of Publication:
United Kingdom
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Hwang, Yunha, Roux, Simon, Coclet, Clément, Krause, Sebastian J. E., and Girguis, Peter R. Viruses interact with hosts that span distantly related microbial domains in dense hydrothermal mats. United Kingdom: N. p., 2023. Web. doi:10.1038/s41564-023-01347-5.
Hwang, Yunha, Roux, Simon, Coclet, Clément, Krause, Sebastian J. E., & Girguis, Peter R. Viruses interact with hosts that span distantly related microbial domains in dense hydrothermal mats. United Kingdom. https://doi.org/10.1038/s41564-023-01347-5
Hwang, Yunha, Roux, Simon, Coclet, Clément, Krause, Sebastian J. E., and Girguis, Peter R. Thu . "Viruses interact with hosts that span distantly related microbial domains in dense hydrothermal mats". United Kingdom. https://doi.org/10.1038/s41564-023-01347-5.
@article{osti_1968630,
title = {Viruses interact with hosts that span distantly related microbial domains in dense hydrothermal mats},
author = {Hwang, Yunha and Roux, Simon and Coclet, Clément and Krause, Sebastian J. E. and Girguis, Peter R.},
abstractNote = {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.},
doi = {10.1038/s41564-023-01347-5},
journal = {Nature Microbiology},
number = 5,
volume = 8,
place = {United Kingdom},
year = {Thu Apr 06 00:00:00 EDT 2023},
month = {Thu Apr 06 00:00:00 EDT 2023}
}

Works referenced in this record:

Networks of energetic and metabolic interactions define dynamics in microbial communities
journal, November 2015

  • Embree, Mallory; Liu, Joanne K.; Al-Bassam, Mahmoud M.
  • Proceedings of the National Academy of Sciences, Vol. 112, Issue 50
  • DOI: 10.1073/pnas.1506034112

It Takes a Village: Microbial Communities Thrive through Interactions and Metabolic Handoffs
journal, March 2018


DRAM for distilling microbial metabolism to automate the curation of microbiome function
journal, August 2020

  • Shaffer, Michael; Borton, Mikayla A.; McGivern, Bridget B.
  • Nucleic Acids Research, Vol. 48, Issue 16
  • DOI: 10.1093/nar/gkaa621

Bacteriophages isolated from Lake Michigan demonstrate broad host-range across several bacterial phyla
journal, October 2015


Genomes OnLine Database (GOLD) v.8: overview and updates
journal, November 2020

  • Mukherjee, Supratim; Stamatis, Dimitri; Bertsch, Jon
  • Nucleic Acids Research, Vol. 49, Issue D1
  • DOI: 10.1093/nar/gkaa983

Spectrophotometric Determination Of Hydrogen Sulfide In Natural Waters
journal, May 1969


High-quality genome sequences of uncultured microbes by assembly of read clouds
journal, October 2018

  • Bishara, Alex; Moss, Eli L.; Kolmogorov, Mikhail
  • Nature Biotechnology, Vol. 36, Issue 11
  • DOI: 10.1038/nbt.4266

Defining the human gut host–phage network through single-cell viral tagging
journal, August 2019


Taxonomic assignment of uncultivated prokaryotic virus genomes is enabled by gene-sharing networks
journal, May 2019


Major bacterial lineages are essentially devoid of CRISPR-Cas viral defence systems
journal, February 2016

  • Burstein, David; Sun, Christine L.; Brown, Christopher T.
  • Nature Communications, Vol. 7, Issue 1
  • DOI: 10.1038/ncomms10613

Lipid analysis of CO2-rich subsurface aquifers suggests an autotrophy-based deep biosphere with lysolipids enriched in CPR bacteria
journal, March 2020

  • Probst, Alexander J.; Elling, Felix J.; Castelle, Cindy J.
  • The ISME Journal, Vol. 14, Issue 6
  • DOI: 10.1038/s41396-020-0624-4

UniRef: comprehensive and non-redundant UniProt reference clusters
journal, March 2007


Understanding the Complex Phage-Host Interactions in Biofilm Communities
journal, September 2021


Reverse Transcriptase-Mediated Tropism Switching in Bordetella Bacteriophage
journal, March 2002


The isolation and characterization of two Stenotrophomonas maltophilia bacteriophages capable of cross-taxonomic order infectivity
journal, September 2015


IMG/VR v3: an integrated ecological and evolutionary framework for interrogating genomes of uncultivated viruses
journal, November 2020

  • Roux, Simon; Páez-Espino, David; Chen, I-Min A.
  • Nucleic Acids Research, Vol. 49, Issue D1
  • DOI: 10.1093/nar/gkaa946

inStrain profiles population microdiversity from metagenomic data and sensitively detects shared microbial strains
journal, January 2021

  • Olm, Matthew R.; Crits-Christoph, Alexander; Bouma-Gregson, Keith
  • Nature Biotechnology, Vol. 39, Issue 6
  • DOI: 10.1038/s41587-020-00797-0

ggplot2
book, January 2016


PHROG: families of prokaryotic virus proteins clustered using remote homology
journal, June 2021

  • Terzian, Paul; Olo Ndela, Eric; Galiez, Clovis
  • NAR Genomics and Bioinformatics, Vol. 3, Issue 3
  • DOI: 10.1093/nargab/lqab067

Marine microbial metagenomes sampled across space and time
journal, September 2018

  • Biller, Steven J.; Berube, Paul M.; Dooley, Keven
  • Scientific Data, Vol. 5, Issue 1
  • DOI: 10.1038/sdata.2018.176

Sulfur Metabolisms in Epsilon- and Gamma-Proteobacteria in Deep-Sea Hydrothermal Fields
journal, January 2011


Inter-phylum HGT has shaped the metabolism of many mesophilic and anaerobic bacteria
journal, October 2014

  • Caro-Quintero, Alejandro; Konstantinidis, Konstantinos T.
  • The ISME Journal, Vol. 9, Issue 4
  • DOI: 10.1038/ismej.2014.193

metaSPAdes: a new versatile metagenomic assembler
journal, March 2017

  • Nurk, Sergey; Meleshko, Dmitry; Korobeynikov, Anton
  • Genome Research, Vol. 27, Issue 5
  • DOI: 10.1101/gr.213959.116

MetaCRAST: reference-guided extraction of CRISPR spacers from unassembled metagenomes
journal, January 2017


CD-HIT: accelerated for clustering the next-generation sequencing data
journal, October 2012


Microbial Communities of Hydrothermal Guaymas Basin Surficial Sediment Profiled at 2 Millimeter-Scale Resolution
journal, July 2021


Normalizing Metagenomic Hi-C Data and Detecting Spurious Contacts Using Zero-Inflated Negative Binomial Regression
journal, February 2022

  • Du, Yuxuan; Laperriere, Sarah M.; Fuhrman, Jed
  • Journal of Computational Biology, Vol. 29, Issue 2
  • DOI: 10.1089/cmb.2021.0439

Prodigal: prokaryotic gene recognition and translation initiation site identification
journal, March 2010


MaxBin 2.0: an automated binning algorithm to recover genomes from multiple metagenomic datasets
journal, October 2015


HMMER web server: 2018 update
journal, June 2018

  • Potter, Simon C.; Luciani, Aurélien; Eddy, Sean R.
  • Nucleic Acids Research, Vol. 46, Issue W1
  • DOI: 10.1093/nar/gky448

Minimum Information about an Uncultivated Virus Genome (MIUViG)
journal, December 2018

  • Roux, Simon; Adriaenssens, Evelien M.; Dutilh, Bas E.
  • Nature Biotechnology, Vol. 37, Issue 1
  • DOI: 10.1038/nbt.4306

CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes
journal, May 2015

  • Parks, Donovan H.; Imelfort, Michael; Skennerton, Connor T.
  • Genome Research, Vol. 25, Issue 7
  • DOI: 10.1101/gr.186072.114

Co-Correspondence Analysis: a new Ordination Method to Relate two Community Compositions
journal, March 2004

  • ter Braak, Cajo J. F.; Schaffers, André P.
  • Ecology, Vol. 85, Issue 3
  • DOI: 10.1890/03-0021

Fast and sensitive protein alignment using DIAMOND
journal, November 2014

  • Buchfink, Benjamin; Xie, Chao; Huson, Daniel H.
  • Nature Methods, Vol. 12, Issue 1
  • DOI: 10.1038/nmeth.3176

Interdomain Conjugal Transfer of DNA from Bacteria to Archaea
journal, June 2010

  • Dodsworth, J. A.; Li, L.; Wei, S.
  • Applied and Environmental Microbiology, Vol. 76, Issue 16
  • DOI: 10.1128/AEM.00967-10

MetaHiC phage-bacteria infection network reveals active cycling phages of the healthy human gut
journal, February 2021


Recovery of genomes from metagenomes via a dereplication, aggregation and scoring strategy
journal, May 2018

  • Sieber, Christian M. K.; Probst, Alexander J.; Sharrar, Allison
  • Nature Microbiology, Vol. 3, Issue 7
  • DOI: 10.1038/s41564-018-0171-1

Defensive symbiosis against giant viruses in amoebae
journal, August 2022

  • Arthofer, Patrick; Delafont, Vincent; Willemsen, Anouk
  • Proceedings of the National Academy of Sciences, Vol. 119, Issue 36
  • DOI: 10.1073/pnas.2205856119

VirSorter2: a multi-classifier, expert-guided approach to detect diverse DNA and RNA viruses
journal, February 2021


Uncovering Earth’s virome
journal, August 2016

  • Paez-Espino, David; Eloe-Fadrosh, Emiley A.; Pavlopoulos, Georgios A.
  • Nature, Vol. 536, Issue 7617
  • DOI: 10.1038/nature19094

Prokka: rapid prokaryotic genome annotation
journal, March 2014


A distinct lineage of Caudovirales that encodes a deeply branching multi-subunit RNA polymerase
journal, September 2020


Genomic insights into potential interdependencies in microbial hydrocarbon and nutrient cycling in hydrothermal sediments
journal, August 2017


Multi-species host range of staphylococcal phages isolated from wastewater
journal, November 2021


vRhyme enables binning of viral genomes from metagenomes
journal, May 2022

  • Kieft, Kristopher; Adams, Alyssa; Salamzade, Rauf
  • Nucleic Acids Research, Vol. 50, Issue 14
  • DOI: 10.1093/nar/gkac341

Prokaryotic Virus Orthologous Groups (pVOGs): a resource for comparative genomics and protein family annotation
journal, October 2016

  • Grazziotin, Ana Laura; Koonin, Eugene V.; Kristensen, David M.
  • Nucleic Acids Research, Vol. 45, Issue D1
  • DOI: 10.1093/nar/gkw975

Bacteria and archaea on Earth and their abundance in biofilms
journal, February 2019


Binning metagenomic contigs by coverage and composition
journal, September 2014

  • Alneberg, Johannes; Bjarnason, Brynjar Smári; de Bruijn, Ino
  • Nature Methods, Vol. 11, Issue 11
  • DOI: 10.1038/nmeth.3103

VIBRANT: automated recovery, annotation and curation of microbial viruses, and evaluation of viral community function from genomic sequences
journal, June 2020


MMseqs2 enables sensitive protein sequence searching for the analysis of massive data sets
journal, October 2017

  • Steinegger, Martin; Söding, Johannes
  • Nature Biotechnology, Vol. 35, Issue 11
  • DOI: 10.1038/nbt.3988

Systematic discovery of antiphage defense systems in the microbial pangenome
journal, January 2018


The Repetitive DNA Elements Called CRISPRs and Their Associated Genes: Evidence of Horizontal Transfer Among Prokaryotes
journal, April 2006


Phage–host coevolution in natural populations
journal, June 2022


Global metagenomic survey reveals a new bacterial candidate phylum in geothermal springs
journal, January 2016

  • Eloe-Fadrosh, Emiley A.; Paez-Espino, David; Jarett, Jessica
  • Nature Communications, Vol. 7, Issue 1
  • DOI: 10.1038/ncomms10476

Adaptation in bacterial CRISPR-Cas immunity can be driven by defective phages
journal, July 2014

  • Hynes, Alexander P.; Villion, Manuela; Moineau, Sylvain
  • Nature Communications, Vol. 5, Issue 1
  • DOI: 10.1038/ncomms5399

Novel syntrophic bacteria in full-scale anaerobic digesters revealed by genome-centric metatranscriptomics
journal, January 2020

  • Hao, Liping; Michaelsen, Thomas Yssing; Singleton, Caitlin Margaret
  • The ISME Journal, Vol. 14, Issue 4
  • DOI: 10.1038/s41396-019-0571-0

Cytoscape: A Software Environment for Integrated Models of Biomolecular Interaction Networks
journal, November 2003


The pan-immune system of bacteria: antiviral defence as a community resource
journal, November 2019


A marine microbial consortium apparently mediating anaerobic oxidation of methane
journal, October 2000

  • Boetius, Antje; Ravenschlag, Katrin; Schubert, Carsten J.
  • Nature, Vol. 407, Issue 6804
  • DOI: 10.1038/35036572

Evaluation of microbial biofilm communities from an Alberta oil sands tailings pond
journal, November 2011


Basic local alignment search tool
journal, October 1990

  • Altschul, Stephen F.; Gish, Warren; Miller, Webb
  • Journal of Molecular Biology, Vol. 215, Issue 3, p. 403-410
  • DOI: 10.1016/S0022-2836(05)80360-2

dRep: a tool for fast and accurate genomic comparisons that enables improved genome recovery from metagenomes through de-replication
journal, July 2017

  • Olm, Matthew R.; Brown, Christopher T.; Brooks, Brandon
  • The ISME Journal, Vol. 11, Issue 12
  • DOI: 10.1038/ismej.2017.126

Extracellular electron uptake in Methanosarcinales is independent of multiheme c-type cytochromes
journal, January 2020


CheckV assesses the quality and completeness of metagenome-assembled viral genomes
journal, December 2020

  • Nayfach, Stephen; Camargo, Antonio Pedro; Schulz, Frederik
  • Nature Biotechnology, Vol. 39, Issue 5
  • DOI: 10.1038/s41587-020-00774-7

Understanding Bacteriophage Specificity in Natural Microbial Communities
journal, March 2013


The Thermotoga maritima Phenotype Is Impacted by Syntrophic Interaction with Methanococcus jannaschii in Hyperthermophilic Coculture
journal, January 2006


An oligotrophic deep-subsurface community dependent on syntrophy is dominated by sulfur-driven autotrophic denitrifiers
journal, November 2016

  • Lau, Maggie C. Y.; Kieft, Thomas L.; Kuloyo, Olukayode
  • Proceedings of the National Academy of Sciences, Vol. 113, Issue 49
  • DOI: 10.1073/pnas.1612244113

Diverse Viruses Carrying Genes for Microbial Extremotolerance in the Atacama Desert Hyperarid Soil
journal, June 2021


Organic carbon production, mineralisation and preservation on the Peruvian margin
journal, March 2015


Systematic and quantitative view of the antiviral arsenal of prokaryotes
journal, May 2022


The COG database: an updated version includes eukaryotes
journal, January 2003

  • Tatusov, Roman L.; Fedorova, Natalie D.; Jackson, John D.
  • BMC Bioinformatics, Vol. 4, Article No. 41
  • DOI: 10.1186/1471-2105-4-41

CRISPRCasFinder, an update of CRISRFinder, includes a portable version, enhanced performance and integrates search for Cas proteins
journal, May 2018

  • Couvin, David; Bernheim, Aude; Toffano-Nioche, Claire
  • Nucleic Acids Research, Vol. 46, Issue W1
  • DOI: 10.1093/nar/gky425

MetaBAT 2: an adaptive binning algorithm for robust and efficient genome reconstruction from metagenome assemblies
journal, January 2019


Patterns of syntrophic interactions in methanogenic conversion of propionate
journal, October 2021


Functional Insights of Salinity Stress-Related Pathways in Metagenome-Resolved Methanothrix Genomes
journal, May 2022

  • Gagliano, Maria Cristina; Sampara, Pranav; Plugge, Caroline M.
  • Applied and Environmental Microbiology, Vol. 88, Issue 10
  • DOI: 10.1128/aem.02449-21

bin3C: exploiting Hi-C sequencing data to accurately resolve metagenome-assembled genomes
journal, February 2019


Extensive diversity and rapid turnover of phage defense repertoires in cheese-associated bacterial communities
journal, August 2022