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Title: Viral elements and their potential influence on microbial processes along the permanently stratified Cariaco Basin redoxcline

Abstract

Little is known about viruses in oxygen-deficient water columns (ODWCs). In surface ocean waters, viruses are known to act as gene vectors among susceptible hosts. Some of these genes may have metabolic functions and are thus termed auxiliary metabolic genes (AMGs). AMGs introduced to new hosts by viruses can enhance viral replication and/or potentially affect biogeochemical cycles by modulating key microbial pathways. Here we identify 748 viral populations that cluster into 94 genera along a vertical geochemical gradient in the Cariaco Basin, a permanently stratified and euxinic ocean basin. The viral communities in this ODWC appear to be relatively novel as 80 of these viral genera contained no reference viral sequences, likely due to the isolation and unique features of this system. We identify viral elements that encode AMGs implicated in distinctive processes, such as sulfur cycling, acetate fermentation, signal transduction, [Fe–S] formation, and N-glycosylation. These AMG-encoding viruses include two putative Mu-like viruses, and viral-like regions that may constitute degraded prophages that have been modified by transposable elements. Our results provide an insight into the ecological and biogeochemical impact of viruses oxygen-depleted and euxinic habitats.

Authors:
ORCiD logo [1]; ORCiD logo [2]; ORCiD logo [3]; ORCiD logo [4];  [5]; ORCiD logo [6];  [7]; ORCiD logo [1]
+ Show Author Affiliations
  1. Woods Hole Oceanographic Institution, Woods Hole, MA (United States). Geology and Geophysics Dept.
  2. The Ohio State Univ., Columbus, OH (United States). Dept. of Microbiology
  3. Woods Hole Oceanographic Institution, Woods Hole, MA (United States). Biology Dept.
  4. Molloy College, Rockville Centre, NY (United States). Biology, Chemistry, and Environmental Studies Dept.
  5. Univ. of Arizona, Tucson, AZ (United States). Dept. of Ecology and Evolutionary Biology
  6. Stony Brook Univ., NY (United States). School of Marine and Atmospheric Sciences
  7. The Ohio State Univ., Columbus, OH (United States). Dept. of Microbiology; The Ohio State Univ., Columbus, OH (United States). Dept. of Civil, Environmental and Geodetic Engineering
Publication Date:
Research Org.:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). National Energy Research Scientific Computing Center (NERSC)
Sponsoring Org.:
USDOE Office of Science (SC); National Science Foundation (NSF)
OSTI Identifier:
1817130
Grant/Contract Number:  
AC02-05CH11231; OCE-1336082; OCE-1335436; OCE-1536989; 3790
Resource Type:
Accepted Manuscript
Journal Name:
The ISME Journal
Additional Journal Information:
Journal Volume: 14; Journal Issue: 12; Journal ID: ISSN 1751-7362
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; metagenomics; microbial ecology

Citation Formats

Mara, Paraskevi, Vik, Dean, Pachiadaki, Maria G., Suter, Elizabeth A., Poulos, Bonnie, Taylor, Gordon T., Sullivan, Matthew B., and Edgcomb, Virginia P. Viral elements and their potential influence on microbial processes along the permanently stratified Cariaco Basin redoxcline. United States: N. p., 2020. Web. doi:10.1038/s41396-020-00739-3.
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Mara, Paraskevi, Vik, Dean, Pachiadaki, Maria G., Suter, Elizabeth A., Poulos, Bonnie, Taylor, Gordon T., Sullivan, Matthew B., & Edgcomb, Virginia P. Viral elements and their potential influence on microbial processes along the permanently stratified Cariaco Basin redoxcline. United States. https://doi.org/10.1038/s41396-020-00739-3
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Mara, Paraskevi, Vik, Dean, Pachiadaki, Maria G., Suter, Elizabeth A., Poulos, Bonnie, Taylor, Gordon T., Sullivan, Matthew B., and Edgcomb, Virginia P. Fri . "Viral elements and their potential influence on microbial processes along the permanently stratified Cariaco Basin redoxcline". United States. https://doi.org/10.1038/s41396-020-00739-3. https://www.osti.gov/servlets/purl/1817130.
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@article{osti_1817130,
title = {Viral elements and their potential influence on microbial processes along the permanently stratified Cariaco Basin redoxcline},
author = {Mara, Paraskevi and Vik, Dean and Pachiadaki, Maria G. and Suter, Elizabeth A. and Poulos, Bonnie and Taylor, Gordon T. and Sullivan, Matthew B. and Edgcomb, Virginia P.},
abstractNote = {Little is known about viruses in oxygen-deficient water columns (ODWCs). In surface ocean waters, viruses are known to act as gene vectors among susceptible hosts. Some of these genes may have metabolic functions and are thus termed auxiliary metabolic genes (AMGs). AMGs introduced to new hosts by viruses can enhance viral replication and/or potentially affect biogeochemical cycles by modulating key microbial pathways. Here we identify 748 viral populations that cluster into 94 genera along a vertical geochemical gradient in the Cariaco Basin, a permanently stratified and euxinic ocean basin. The viral communities in this ODWC appear to be relatively novel as 80 of these viral genera contained no reference viral sequences, likely due to the isolation and unique features of this system. We identify viral elements that encode AMGs implicated in distinctive processes, such as sulfur cycling, acetate fermentation, signal transduction, [Fe–S] formation, and N-glycosylation. These AMG-encoding viruses include two putative Mu-like viruses, and viral-like regions that may constitute degraded prophages that have been modified by transposable elements. Our results provide an insight into the ecological and biogeochemical impact of viruses oxygen-depleted and euxinic habitats.},
doi = {10.1038/s41396-020-00739-3},
journal = {The ISME Journal},
number = 12,
volume = 14,
place = {United States},
year = {Fri Aug 14 00:00:00 EDT 2020},
month = {Fri Aug 14 00:00:00 EDT 2020}
}
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https://doi.org/10.1038/s41396-020-00739-3
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Works referenced in this record:

Benchmarking viromics: an in silico evaluation of metagenome-enabled estimates of viral community composition and diversity
journal, January 2017

  • Roux, Simon; Emerson, Joanne B.; Eloe-Fadrosh, Emiley A.
  • PeerJ, Vol. 5
  • DOI: 10.7717/peerj.3817

A new perspective on lysogeny: prophages as active regulatory switches of bacteria
journal, September 2015

  • Feiner, Ron; Argov, Tal; Rabinovich, Lev
  • Nature Reviews Microbiology, Vol. 13, Issue 10
  • DOI: 10.1038/nrmicro3527

Novel Stenotrophomonas maltophilia temperate phage DLP4 is capable of lysogenic conversion
journal, April 2019

Sulfur Oxidation Genes in Diverse Deep-Sea Viruses
journal, May 2014

Oxygen minimum zones harbour novel viral communities with low diversity: Viral community characteristics of an oxygen minimum zone
journal, October 2012

Versatile and open software for comparing large genomes
journal, January 2004

  • Kurtz, Stefan; Phillippy, Adam; Delcher, Arthur L.
  • Genome Biology, Vol. 5, Issue 2, R12
  • DOI: 10.1186/gb-2004-5-2-r12

Comparative Omics and Trait Analyses of Marine Pseudoalteromonas Phages Advance the Phage OTU Concept
journal, July 2017

Structure, Function, and Formation of Biological Iron-Sulfur Clusters
journal, June 2005

A bioinformatic analysis of ribonucleotide reductase genes in phage genomes and metagenomes
journal, January 2013

  • Dwivedi, Bhakti; Xue, Bingjie; Lundin, Daniel
  • BMC Evolutionary Biology, Vol. 13, Issue 1
  • DOI: 10.1186/1471-2148-13-33

Molecular model for the transposition and replication of bacteriophage Mu and other transposable elements.
journal, April 1979

  • Shapiro, J. A.
  • Proceedings of the National Academy of Sciences, Vol. 76, Issue 4
  • DOI: 10.1073/pnas.76.4.1933

Depth-stratified functional and taxonomic niche specialization in the ‘core’ and ‘flexible’ Pacific Ocean Virome
journal, August 2014

  • Hurwitz, Bonnie L.; Brum, Jennifer R.; Sullivan, Matthew B.
  • The ISME Journal, Vol. 9, Issue 2
  • DOI: 10.1038/ismej.2014.143

Marine Viruses Exploit Their Host's Two-Component Regulatory System in Response to Resource Limitation
journal, January 2012

Pvclust: an R package for assessing the uncertainty in hierarchical clustering
journal, April 2006

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

Acetate cycling in the water column of the Cariaco Basin: Seasonal and vertical variability and implication for carbon cycling
journal, July 2002

  • Ho, Tung-Yuan; Scranton, Mary I.; Taylor, Gordon T.
  • Limnology and Oceanography, Vol. 47, Issue 4
  • DOI: 10.4319/lo.2002.47.4.1119

Gene and translation initiation site prediction in metagenomic sequences
journal, July 2012

Discovery of several novel, widespread, and ecologically distinct marine Thaumarchaeota viruses that encode amoC nitrification genes
journal, October 2018

Phage puppet masters of the marine microbial realm
journal, June 2018

Genomic differentiation among wild cyanophages despite widespread horizontal gene transfer
journal, November 2016

  • Gregory, Ann C.; Solonenko, Sergei A.; Ignacio-Espinoza, J. Cesar
  • BMC Genomics, Vol. 17, Issue 1
  • DOI: 10.1186/s12864-016-3286-x

Comparative metagenomic analyses reveal viral-induced shifts of host metabolism towards nucleotide biosynthesis
journal, January 2014

  • Enav, Hagay; Mandel-Gutfreund, Yael; Béjà, Oded
  • Microbiome, Vol. 2, Issue 1
  • DOI: 10.1186/2049-2618-2-9

Novel Abundant Oceanic Viruses of Uncultured Marine Group II Euryarchaeota
journal, May 2017

Biopython: freely available Python tools for computational molecular biology and bioinformatics
journal, March 2009

Microbial metabolisms in a 2.5-km-deep ecosystem created by hydraulic fracturing in shales
journal, September 2016

Trimmomatic: a flexible trimmer for Illumina sequence data
journal, April 2014

The Phyre2 web portal for protein modeling, prediction and analysis
journal, May 2015

  • Kelley, Lawrence A.; Mezulis, Stefans; Yates, Christopher M.
  • Nature Protocols, Vol. 10, Issue 6
  • DOI: 10.1038/nprot.2015.053

Patterns and ecological drivers of ocean viral communities
journal, May 2015

Novel chaperonins are prevalent in the virioplankton and demonstrate links to viral biology and ecology
journal, July 2017

  • Marine, Rachel L.; Nasko, Daniel J.; Wray, Jeffrey
  • The ISME Journal, Vol. 11, Issue 11
  • DOI: 10.1038/ismej.2017.102

Genome and physiology of a model Epsilonproteobacterium responsible for sulfide detoxification in marine oxygen depletion zones
journal, December 2011

  • Grote, J.; Schott, T.; Bruckner, C. G.
  • Proceedings of the National Academy of Sciences, Vol. 109, Issue 2
  • DOI: 10.1073/pnas.1111262109

Chemoautotrophy in the redox transition zone of the Cariaco Basin: A significant midwater source of organic carbon production
journal, January 2001

  • Taylor, Gordon T.; Iabichella, Maria; Ho, Tung-Yuan
  • Limnology and Oceanography, Vol. 46, Issue 1
  • DOI: 10.4319/lo.2001.46.1.0148

Marine DNA Viral Macro- and Microdiversity from Pole to Pole
journal, May 2019

A new component of bacteriophage Mu replicative transposition machinery: the Escherichia coli ClpX protein
journal, March 1994

Gene transfer agents: phage-like elements of genetic exchange
journal, June 2012

  • Lang, Andrew S.; Zhaxybayeva, Olga; Beatty, J. Thomas
  • Nature Reviews Microbiology, Vol. 10, Issue 7
  • DOI: 10.1038/nrmicro2802

A simple and efficient method for concentration of ocean viruses by chemical flocculation: Virus concentration by flocculation with iron
journal, August 2010

The HIRAN Domain and Recruitment of Chromatin Remodeling and Repair activities to Damaged DNA
journal, March 2006

  • Iyer, Lakshminarayan M.; Babu, Madan; Aravind, L.
  • Cell Cycle, Vol. 5, Issue 7
  • DOI: 10.4161/cc.5.7.2629

Controls on temporal variability of the geochemistry of the deep Cariaco Basin
journal, July 2001

  • Scranton, Mary I.; Astor, Yrene; Bohrer, Richard
  • Deep Sea Research Part I: Oceanographic Research Papers, Vol. 48, Issue 7
  • DOI: 10.1016/S0967-0637(00)00087-X

Putative archaeal viruses from the mesopelagic ocean
journal, January 2017

Recombination and Recombination-Dependent dna Replication in Bacteriophage t4
journal, December 1998

Glycosylation-directed quality control of protein folding
journal, October 2015

  • Xu, Chengchao; Ng, Davis T. W.
  • Nature Reviews Molecular Cell Biology, Vol. 16, Issue 12
  • DOI: 10.1038/nrm4073

Temporal variations in viral distributions in the anoxic Cariaco Basin
journal, January 2003

  • Taylor, Gt; Hein, C.; Iabichella, M.
  • Aquatic Microbial Ecology, Vol. 30
  • DOI: 10.3354/ame030103

PHASTER: a better, faster version of the PHAST phage search tool
journal, May 2016

  • Arndt, David; Grant, Jason R.; Marcu, Ana
  • Nucleic Acids Research, Vol. 44, Issue W1
  • DOI: 10.1093/nar/gkw387

Ecogenomics and potential biogeochemical impacts of globally abundant ocean viruses
journal, September 2016

  • Roux, Simon; Brum, Jennifer R.; Dutilh, Bas E.
  • Nature, Vol. 537, Issue 7622
  • DOI: 10.1038/nature19366

Interannual and Subdecadal Variability in the Nutrient Geochemistry of the Cariaco Basin
journal, March 2014

Easyfig: a genome comparison visualizer
journal, January 2011

Molecular determinant of the effects of hydrostatic pressure on protein folding stability
journal, February 2017

  • Chen, Calvin R.; Makhatadze, George I.
  • Nature Communications, Vol. 8, Issue 1
  • DOI: 10.1038/ncomms14561

VirSorter: mining viral signal from microbial genomic data
journal, January 2015

  • Roux, Simon; Enault, Francois; Hurwitz, Bonnie L.
  • PeerJ, Vol. 3
  • DOI: 10.7717/peerj.985

Hydrolytic ectoenzyme activity associated with suspended and sinking organic particles within the anoxic Cariaco Basin
journal, August 2009

  • Taylor, Gordon T.; Thunell, Robert; Varela, Ramon
  • Deep Sea Research Part I: Oceanographic Research Papers, Vol. 56, Issue 8
  • DOI: 10.1016/j.dsr.2009.02.006

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

An intriguing relationship between the cyclic diguanylate signaling system and horizontal gene transfer
journal, June 2018

Archaeal S-layer glycoproteins: post-translational modification in the face of extremes
journal, November 2014

Genomic analysis of oceanic cyanobacterial myoviruses compared with T4-like myoviruses from diverse hosts and environments: Comparative genomics of T4-like myoviruses
journal, November 2010

Metabolic reprogramming by viruses in the sunlit and dark ocean
journal, January 2013

Characterization of a newly discovered Mu-like bacteriophage, RcapMu, in Rhodobacter capsulatus strain SB1003
journal, December 2011

A role for the Clp protease in activating Mu-mediated DNA rearrangements
journal, May 1993

Exploring the Vast Diversity of Marine Viruses
journal, June 2007

Decline in global oceanic oxygen content during the past five decades
journal, February 2017

  • Schmidtko, Sunke; Stramma, Lothar; Visbeck, Martin
  • Nature, Vol. 542, Issue 7641
  • DOI: 10.1038/nature21399

Genome-wide expression dynamics of a marine virus and host reveal features of co-evolution
journal, September 2007

  • Lindell, Debbie; Jaffe, Jacob D.; Coleman, Maureen L.
  • Nature, Vol. 449, Issue 7158
  • DOI: 10.1038/nature06130

Biomarkers, chemistry and microbiology show chemoautotrophy in a multilayer chemocline in the Cariaco Basin
journal, May 2012

  • Wakeham, Stuart G.; Turich, Courtney; Schubotz, Florence
  • Deep Sea Research Part I: Oceanographic Research Papers, Vol. 63
  • DOI: 10.1016/j.dsr.2012.01.005

Life-Cycle and Genome of OtV5, a Large DNA Virus of the Pelagic Marine Unicellular Green Alga Ostreococcus tauri
journal, May 2008

Comparative metagenomics of microbial traits within oceanic viral communities
journal, February 2011

  • Sharon, Itai; Battchikova, Natalia; Aro, Eva-Mari
  • The ISME Journal, Vol. 5, Issue 7
  • DOI: 10.1038/ismej.2011.2

Prevalence and Evolution of Core Photosystem II Genes in Marine Cyanobacterial Viruses and Their Hosts
journal, July 2006

Phage-specific metabolic reprogramming of virocells
journal, January 2020

  • Howard-Varona, Cristina; Lindback, Morgan M.; Bastien, G. Eric
  • The ISME Journal, Vol. 14, Issue 4
  • DOI: 10.1038/s41396-019-0580-z

Three Prochlorococcus Cyanophage Genomes: Signature Features and Ecological Interpretations
journal, April 2005

PhageTerm: a tool for fast and accurate determination of phage termini and packaging mechanism using next-generation sequencing data
journal, August 2017

  • Garneau, Julian R.; Depardieu, Florence; Fortier, Louis-Charles
  • Scientific Reports, Vol. 7, Issue 1
  • DOI: 10.1038/s41598-017-07910-5

Temporal changes in the hydrography and chemistry of the Cariaco Trench
journal, May 1987

  • Scranton, Mary I.; Sayles, Frederick L.; Bacon, Michael P.
  • Deep Sea Research Part A. Oceanographic Research Papers, Vol. 34, Issue 5-6
  • DOI: 10.1016/0198-0149(87)90047-1

The distribution and cycling of hydrogen gas in the waters of two anoxic marine environments1,2: H 2 in two anoxic systems
journal, September 1984

  • Scranton, Mary I.; Novelli, Paul C.; Loud, Peter A.
  • Limnology and Oceanography, Vol. 29, Issue 5
  • DOI: 10.4319/lo.1984.29.5.0993

VirFinder: a novel k-mer based tool for identifying viral sequences from assembled metagenomic data
journal, July 2017

Prophage deletion mapping of bacteriophage Mu-1
journal, July 1973

Phylogenetic Diversity of Bacterial and Archaeal Communities in the Anoxic Zone of the Cariaco Basin
journal, April 2001

Modeling the Fitness Consequences of a Cyanophage-Encoded Photosynthesis Gene
journal, October 2008

The Acetate Switch
journal, March 2005

Microbial niches in marine oxygen minimum zones
journal, September 2018

Recognition of prokaryotic and eukaryotic promoters using convolutional deep learning neural networks
journal, February 2017

Robust estimation of microbial diversity in theory and in practice
journal, February 2013

  • Haegeman, Bart; Hamelin, Jérôme; Moriarty, John
  • The ISME Journal, Vol. 7, Issue 6
  • DOI: 10.1038/ismej.2013.10

The genome and structural proteome of an ocean siphovirus: a new window into the cyanobacterial ‘mobilome’
journal, November 2009

Functional analysis of N-linking oligosaccharyl transferase enzymes encoded by deep-sea vent proteobacteria
journal, November 2015

  • Mills, Dominic C.; Jervis, Adrian J.; Abouelhadid, Sherif
  • Glycobiology, Vol. 26, Issue 4
  • DOI: 10.1093/glycob/cwv111

Ecology of prokaryotic viruses
journal, May 2004

Two recombination-dependent DNA replication pathways of bacteriophage T4, and their roles in mutagenesis and horizontal gene transfer
journal, July 2001

  • Mosig, G.; Gewin, J.; Luder, A.
  • Proceedings of the National Academy of Sciences, Vol. 98, Issue 15
  • DOI: 10.1073/pnas.131007398

Principles of c-di-GMP signalling in bacteria
journal, April 2009

VEGAN, a package of R functions for community ecology
journal, April 2003

Marine Viruses: Truth or Dare
journal, January 2012

Effects of N-glycosylation on protein conformation and dynamics: Protein Data Bank analysis and molecular dynamics simulation study
journal, March 2015

  • Lee, Hui Sun; Qi, Yifei; Im, Wonpil
  • Scientific Reports, Vol. 5, Issue 1
  • DOI: 10.1038/srep08926

Ocean viruses: Rigorously evaluating the metagenomic sample-to-sequence pipeline
journal, December 2012

Protein glycosylation in bacteria: sweeter than ever
journal, October 2010

  • Nothaft, Harald; Szymanski, Christine M.
  • Nature Reviews Microbiology, Vol. 8, Issue 11
  • DOI: 10.1038/nrmicro2383

Marine viruses and their biogeochemical and ecological effects
journal, June 1999

  • Fuhrman, Jed A.
  • Nature, Vol. 399, Issue 6736
  • DOI: 10.1038/21119

Ecology and evolution of viruses infecting uncultivated SUP05 bacteria as revealed by single-cell- and meta-genomics
journal, August 2014

A high-resolution Late Quaternary upwelling record from the anoxic Cariaco Basin, Venezuela
journal, February 1991

  • Peterson, L. C.; Overpeck, J. T.; Kipp, N. G.
  • Paleoceanography, Vol. 6, Issue 1
  • DOI: 10.1029/90PA02497

Protein acetylation dynamics in response to carbon overflow in E scherichia coli : Acetylation dynamics and overflow metabolism
journal, September 2015

  • Schilling, Birgit; Christensen, David; Davis, Robert
  • Molecular Microbiology, Vol. 98, Issue 5
  • DOI: 10.1111/mmi.13161

Evidence for nifU and nifS Participation in the Biosynthesis of the Iron-Molybdenum Cofactor of Nitrogenase
journal, December 2007

  • Zhao, Dehua; Curatti, Leonardo; Rubio, Luis M.
  • Journal of Biological Chemistry, Vol. 282, Issue 51
  • DOI: 10.1074/jbc.M708097200

Environmental Viral Genomes Shed New Light on Virus-Host Interactions in the Ocean
journal, March 2017

New and continuing developments at PROSITE
journal, November 2012

  • Sigrist, Christian J. A.; de Castro, Edouard; Cerutti, Lorenzo
  • Nucleic Acids Research, Vol. 41, Issue D1
  • DOI: 10.1093/nar/gks1067

Free‐living chemoautotrophic and particle‐attached heterotrophic prokaryotes dominate microbial assemblages along a pelagic redox gradient
journal, December 2017

  • Suter, Elizabeth A.; Pachiadaki, Maria; Taylor, Gordon T.
  • Environmental Microbiology, Vol. 20, Issue 2
  • DOI: 10.1111/1462-2920.13997
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