skip to main content
OSTI.GOV title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Diversity of Active Viral Infections within the Sphagnum Microbiome

Abstract

ABSTRACT Sphagnum-dominated peatlands play an important role in global carbon storage and represent significant sources of economic and ecological value. While recent efforts to describe microbial diversity and metabolic potential of the Sphagnum microbiome have demonstrated the importance of its microbial community, little is known about the viral constituents. We used metatranscriptomics to describe the diversity and activity of viruses infecting microbes within the Sphagnumpeat bog. The vegetative portions of six Sphagnum plants were obtained from a peatland in northern Minnesota, and the total RNA was extracted and sequenced. Metatranscriptomes were assembled and contigs were screened for the presence of conserved virus marker genes. Using bacteriophage capsid protein gp23 as a marker for phage diversity, we identified 33 contigs representing undocumented phages that were active in the community at the time of sampling. Similarly, RNA-dependent RNA polymerase and the nucleocytoplasmic large DNA virus (NCLDV) major capsid protein were used as markers for single-stranded RNA (ssRNA) viruses and NCLDV, respectively. In total, 114 contigs were identified as originating from undescribed ssRNA viruses, 22 of which represent nearly complete genomes. An additional 64 contigs were identified as being from NCLDVs. Finally, 7 contigs were identified as putative virophage or polinton-like viruses. Wemore » developed co-occurrence networks with these markers in relation to the expression of potential-host housekeeping gene rpb1 to predict virus-host relationships, identifying 13 groups. Together, our approach offers new tools for the identification of virus diversity and interactions in understudied clades and suggests that viruses may play a considerable role in the ecology of theSphagnummicrobiome. IMPORTANCE Sphagnum-dominated peatlands play an important role in maintaining atmospheric carbon dioxide levels by modifying conditions in the surrounding soil to favor the growth of over that of other plant species. This lowers the rate of decomposition and facilitates the accumulation of fixed carbon in the form of partially decomposed biomass. The unique environment produced by Sphagnum enriches for the growth of a diverse microbial consortia that benefit from and support the moss's growth, while also maintaining the hostile soil conditions. While a growing body of research has begun to characterize the microbial groups that colonize Sphagnum, little is currently known about the ecological factors that constrain community structure and define ecosystem function. Top-down population control by viruses is almost completely undescribed. Furthermore, this study provides insight into the significant viral influence on the Sphagnum microbiome and identifies new potential model systems to study virus-host interactions in the peatland ecosystem.« less

Authors:
 [1];  [2];  [2]; ORCiD logo [3]; ORCiD logo [3]; ORCiD logo [1];  [4]
  1. Univ. of Tennessee, Knoxville, TN (United States)
  2. Georgia Inst. of Technology, Atlanta, GA (United States)
  3. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
  4. Univ. of Illinois at Urbana-Champaign, Urbana, IL (United States)
Publication Date:
Research Org.:
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
Sponsoring Org.:
USDOE
OSTI Identifier:
1482449
DOE Contract Number:  
AC05-00OR22725
Resource Type:
Journal Article
Journal Name:
Applied and Environmental Microbiology
Additional Journal Information:
Journal Volume: 84; Journal Issue: 23; Journal ID: ISSN 0099-2240
Publisher:
American Society for Microbiology
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; viruses; RNA-Seq; Sphagnum; peat bogs; microbial ecology

Citation Formats

Stough, Joshua M. A., Kolton, Max, Kostka, Joel E., Weston, David J., Pelletier, Dale A., Wilhelm, Steven W., and Cann, Isaac. Diversity of Active Viral Infections within the Sphagnum Microbiome. United States: N. p., 2018. Web. doi:10.1128/AEM.01124-18.
Stough, Joshua M. A., Kolton, Max, Kostka, Joel E., Weston, David J., Pelletier, Dale A., Wilhelm, Steven W., & Cann, Isaac. Diversity of Active Viral Infections within the Sphagnum Microbiome. United States. doi:10.1128/AEM.01124-18.
Stough, Joshua M. A., Kolton, Max, Kostka, Joel E., Weston, David J., Pelletier, Dale A., Wilhelm, Steven W., and Cann, Isaac. Thu . "Diversity of Active Viral Infections within the Sphagnum Microbiome". United States. doi:10.1128/AEM.01124-18.
@article{osti_1482449,
title = {Diversity of Active Viral Infections within the Sphagnum Microbiome},
author = {Stough, Joshua M. A. and Kolton, Max and Kostka, Joel E. and Weston, David J. and Pelletier, Dale A. and Wilhelm, Steven W. and Cann, Isaac},
abstractNote = {ABSTRACT Sphagnum-dominated peatlands play an important role in global carbon storage and represent significant sources of economic and ecological value. While recent efforts to describe microbial diversity and metabolic potential of theSphagnum microbiome have demonstrated the importance of its microbial community, little is known about the viral constituents. We used metatranscriptomics to describe the diversity and activity of viruses infecting microbes within the Sphagnumpeat bog. The vegetative portions of sixSphagnum plants were obtained from a peatland in northern Minnesota, and the total RNA was extracted and sequenced. Metatranscriptomes were assembled and contigs were screened for the presence of conserved virus marker genes. Using bacteriophage capsid protein gp23 as a marker for phage diversity, we identified 33 contigs representing undocumented phages that were active in the community at the time of sampling. Similarly, RNA-dependent RNA polymerase and the nucleocytoplasmic large DNA virus (NCLDV) major capsid protein were used as markers for single-stranded RNA (ssRNA) viruses and NCLDV, respectively. In total, 114 contigs were identified as originating from undescribed ssRNA viruses, 22 of which represent nearly complete genomes. An additional 64 contigs were identified as being from NCLDVs. Finally, 7 contigs were identified as putative virophage or polinton-like viruses. We developed co-occurrence networks with these markers in relation to the expression of potential-host housekeeping gene rpb1 to predict virus-host relationships, identifying 13 groups. Together, our approach offers new tools for the identification of virus diversity and interactions in understudied clades and suggests that viruses may play a considerable role in the ecology of theSphagnummicrobiome. IMPORTANCE Sphagnum-dominated peatlands play an important role in maintaining atmospheric carbon dioxide levels by modifying conditions in the surrounding soil to favor the growth of over that of other plant species. This lowers the rate of decomposition and facilitates the accumulation of fixed carbon in the form of partially decomposed biomass. The unique environment produced by Sphagnum enriches for the growth of a diverse microbial consortia that benefit from and support the moss's growth, while also maintaining the hostile soil conditions. While a growing body of research has begun to characterize the microbial groups that colonize Sphagnum, little is currently known about the ecological factors that constrain community structure and define ecosystem function. Top-down population control by viruses is almost completely undescribed. Furthermore, this study provides insight into the significant viral influence on the Sphagnum microbiome and identifies new potential model systems to study virus-host interactions in the peatland ecosystem.},
doi = {10.1128/AEM.01124-18},
journal = {Applied and Environmental Microbiology},
issn = {0099-2240},
number = 23,
volume = 84,
place = {United States},
year = {2018},
month = {11}
}

Works referenced in this record:

Antibacterial activity of sphagnum acid and other phenolic compounds found in Sphagnum papillosum against food-borne bacteria
journal, July 2009


Global-scale processes with a nanoscale drive: the role of marine viruses
journal, April 2008

  • Brussaard, Corina P. D.; Wilhelm, Steven W.; Thingstad, Frede
  • The ISME Journal, Vol. 2, Issue 6
  • DOI: 10.1038/ismej.2008.31

The ecological significance of organochemical compounds in Sphagnum
journal, June 1997


Metagenomics and biodiversity of sphagnum bogs
journal, September 2016


Attaining whole-ecosystem warming using air and deep-soil heating methods with an elevated CO 2 atmosphere
journal, January 2017

  • Hanson, Paul J.; Riggs, Jeffery S.; Nettles, W. Robert
  • Biogeosciences, Vol. 14, Issue 4
  • DOI: 10.5194/bg-14-861-2017

Metatranscriptome analyses indicate resource partitioning between diatoms in the field
journal, April 2015

  • Alexander, Harriet; Jenkins, Bethany D.; Rynearson, Tatiana A.
  • Proceedings of the National Academy of Sciences, Vol. 112, Issue 17
  • DOI: 10.1073/pnas.1421993112

The elemental composition of virus particles: implications for marine biogeochemical cycles
journal, June 2014

  • Jover, Luis F.; Effler, T. Chad; Buchan, Alison
  • Nature Reviews Microbiology, Vol. 12, Issue 7
  • DOI: 10.1038/nrmicro3289

Soil carbon pools and world life zones
journal, July 1982

  • Post, Wilfred M.; Emanuel, William R.; Zinke, Paul J.
  • Nature, Vol. 298, Issue 5870
  • DOI: 10.1038/298156a0

Cyanophage Diversity, Inferred from g20 Gene Analyses, in the Largest Natural Lake in France, Lake Bourget
journal, February 2004


Ribonucleotide reductases reveal novel viral diversity and predict biological and ecological features of unknown marine viruses
journal, October 2014

  • Sakowski, E. G.; Munsell, E. V.; Hyatt, M.
  • Proceedings of the National Academy of Sciences, Vol. 111, Issue 44
  • DOI: 10.1073/pnas.1401322111

Formation, succession and landscape history of Central-European summit raised bogs: A multiproxy study from the Hrubý Jeseník Mountains
journal, August 2012


New Algorithms and Methods to Estimate Maximum-Likelihood Phylogenies: Assessing the Performance of PhyML 3.0
journal, March 2010

  • Guindon, Stéphane; Dufayard, Jean-François; Lefort, Vincent
  • Systematic Biology, Vol. 59, Issue 3
  • DOI: 10.1093/sysbio/syq010

Eukaryotic large nucleo-cytoplasmic DNA viruses: Clusters of orthologous genes and reconstruction of viral genome evolution
journal, January 2009


Stability of peatland carbon to rising temperatures
journal, December 2016

  • Wilson, R. M.; Hopple, A. M.; Tfaily, M. M.
  • Nature Communications, Vol. 7, Article No. 13723
  • DOI: 10.1038/ncomms13723

Virus taxonomy in the age of metagenomics
journal, January 2017

  • Simmonds, Peter; Adams, Mike J.; Benkő, Mária
  • Nature Reviews Microbiology, Vol. 15, Issue 3
  • DOI: 10.1038/nrmicro.2016.177

Vertical transmission explains the specific Burkholderia pattern in Sphagnum mosses at multi-geographic scale
journal, January 2013

  • Bragina, Anastasia; Cardinale, Massimiliano; Berg, Christian
  • Frontiers in Microbiology, Vol. 4
  • DOI: 10.3389/fmicb.2013.00394

Dynamics of Viral Abundance and Diversity in a Sphagnum-Dominated Peatland: Temporal Fluctuations Prevail Over Habitat
journal, January 2016

  • Ballaud, Flore; Dufresne, Alexis; Francez, André-Jean
  • Frontiers in Microbiology, Vol. 6
  • DOI: 10.3389/fmicb.2015.01494

Northern Peatlands: Role in the Carbon Cycle and Probable Responses to Climatic Warming
journal, May 1991

  • Gorham, Eville
  • Ecological Applications, Vol. 1, Issue 2
  • DOI: 10.2307/1941811

Diversity and comparative genomics of chimeric viruses in Sphagnum- dominated peatlands
journal, July 2016

  • Quaiser, Achim; Krupovic, Mart; Dufresne, Alexis
  • Virus Evolution, Vol. 2, Issue 2
  • DOI: 10.1093/ve/vew025

The Role of Bryophytes in Carbon and Nitrogen Cycling
journal, September 2003

  • Turetsky, Merritt R.
  • The Bryologist, Vol. 106, Issue 3
  • DOI: 10.1639/05

Natural nitrogen filter fails in polluted raised bogs
journal, June 2000


Nitrogen fixation in Sphagnum mosses is affected by moss species and water table level
journal, December 2014


Similar Diversity of Alphaproteobacteria and Nitrogenase Gene Amplicons on Two Related Sphagnum Mosses
journal, January 2012


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

Widespread dust deposition on North American peatlands coincident with European land-clearance
journal, June 2014

  • Ireland, Alex W.; Clifford, Michael J.; Booth, Robert K.
  • Vegetation History and Archaeobotany, Vol. 23, Issue 6
  • DOI: 10.1007/s00334-014-0466-y

Are we missing half of the viruses in the ocean?
journal, November 2012

  • Steward, Grieg F.; Culley, Alexander I.; Mueller, Jaclyn A.
  • The ISME Journal, Vol. 7, Issue 3
  • DOI: 10.1038/ismej.2012.121

Assessing the Diversity and Specificity of Two Freshwater Viral Communities through Metagenomics
journal, March 2012


RNA viruses as major contributors to Antarctic virioplankton: RNA viruses in the Antarctic
journal, April 2016

  • Miranda, Jaclyn A.; Culley, Alexander I.; Schvarcz, Christopher R.
  • Environmental Microbiology, Vol. 18, Issue 11
  • DOI: 10.1111/1462-2920.13291

The Sphagnum microbiome: new insights from an ancient plant lineage
journal, February 2016

  • Kostka, Joel E.; Weston, David J.; Glass, Jennifer B.
  • New Phytologist, Vol. 211, Issue 1
  • DOI: 10.1111/nph.13993

The “Giant Virus Finder” discovers an abundance of giant viruses in the Antarctic dry valleys
journal, February 2017


Diversity and comparative genomics of Microviridae in Sphagnum- dominated peatlands
journal, April 2015


Microbial Metabolic Potential for Carbon Degradation and Nutrient (Nitrogen and Phosphorus) Acquisition in an Ombrotrophic Peatland
journal, March 2014

  • Lin, Xueju; Tfaily, Malak M.; Green, Stefan J.
  • Applied and Environmental Microbiology, Vol. 80, Issue 11
  • DOI: 10.1128/AEM.00206-14

The resilience and functional role of moss in boreal and arctic ecosystems: Tansley review
journal, August 2012


Diversity and Antagonistic Potential of Bacteria Associated with Bryophytes from Nutrient-Poor Habitats of the Baltic Sea Coast
journal, November 2004


Molybdenum-Based Diazotrophy in a Sphagnum Peatland in Northern Minnesota
journal, June 2017

  • Warren, Melissa J.; Lin, Xueju; Gaby, John C.
  • Applied and Environmental Microbiology, Vol. 83, Issue 17
  • DOI: 10.1128/AEM.01174-17

Flow cytometric detection and enumeration of DNA and RNA viruses infecting marine eukaryotic microalgae
journal, April 2007


InterPro in 2017—beyond protein family and domain annotations
journal, November 2016

  • Finn, Robert D.; Attwood, Teresa K.; Babbitt, Patricia C.
  • Nucleic Acids Research, Vol. 45, Issue D1
  • DOI: 10.1093/nar/gkw1107

Virus-host relationships of marine single-celled eukaryotes resolved from metatranscriptomics
journal, June 2017

  • Moniruzzaman, Mohammad; Wurch, Louie L.; Alexander, Harriet
  • Nature Communications, Vol. 8, Issue 1
  • DOI: 10.1038/ncomms16054

CDD: NCBI's conserved domain database
journal, November 2014

  • Marchler-Bauer, Aron; Derbyshire, Myra K.; Gonzales, Noreen R.
  • Nucleic Acids Research, Vol. 43, Issue D1
  • DOI: 10.1093/nar/gku1221

Interactive tree of life (iTOL) v3: an online tool for the display and annotation of phylogenetic and other trees
journal, April 2016

  • Letunic, Ivica; Bork, Peer
  • Nucleic Acids Research, Vol. 44, Issue W1
  • DOI: 10.1093/nar/gkw290

IBS: an illustrator for the presentation and visualization of biological sequences: Fig. 1.
journal, June 2015


Polintons: a hotbed of eukaryotic virus, transposon and plasmid evolution
journal, December 2014

  • Krupovic, Mart; Koonin, Eugene V.
  • Nature Reviews Microbiology, Vol. 13, Issue 2
  • DOI: 10.1038/nrmicro3389

A Student’s Guide to Giant Viruses Infecting Small Eukaryotes: From Acanthamoeba to Zooxanthellae
journal, March 2017

  • Wilhelm, Steven; Bird, Jordan; Bonifer, Kyle
  • Viruses, Vol. 9, Issue 3
  • DOI: 10.3390/v9030046

Giant viruses with an expanded complement of translation system components
journal, April 2017


SortMeRNA: fast and accurate filtering of ribosomal RNAs in metatranscriptomic data
journal, October 2012


The Pfam protein families database: towards a more sustainable future
journal, December 2015

  • Finn, Robert D.; Coggill, Penelope; Eberhardt, Ruth Y.
  • Nucleic Acids Research, Vol. 44, Issue D1
  • DOI: 10.1093/nar/gkv1344

Theoretical models for the control of bacterial growth rate, abundance, diversity and carbon demand
journal, January 1997

  • Thingstad, Tf; Lignell, R.
  • Aquatic Microbial Ecology, Vol. 13
  • DOI: 10.3354/ame013019

Reference sequence (RefSeq) database at NCBI: current status, taxonomic expansion, and functional annotation
journal, November 2015

  • O'Leary, Nuala A.; Wright, Mathew W.; Brister, J. Rodney
  • Nucleic Acids Research, Vol. 44, Issue D1
  • DOI: 10.1093/nar/gkv1189

Genome of brown tide virus (AaV), the little giant of the Megaviridae, elucidates NCLDV genome expansion and host–virus coevolution
journal, October 2014


An enzymic 'latch' on a global carbon store
journal, January 2001

  • Freeman, Chris; Ostle, Nick; Kang, Hojeong
  • Nature, Vol. 409, Issue 6817
  • DOI: 10.1038/35051650

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


The Capsid of the T4 Phage Superfamily: The Evolution, Diversity, and Structure of Some of the Most Prevalent Proteins in the Biosphere
journal, April 2008

  • Comeau, A. M.; Krisch, H. M.
  • Molecular Biology and Evolution, Vol. 25, Issue 7
  • DOI: 10.1093/molbev/msn080

Viruses and Nutrient Cycles in the Sea
journal, October 1999

  • Wilhelm, Steven W.; Suttle, Curtis A.
  • BioScience, Vol. 49, Issue 10
  • DOI: 10.2307/1313569

MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets
journal, March 2016

  • Kumar, Sudhir; Stecher, Glen; Tamura, Koichiro
  • Molecular Biology and Evolution, Vol. 33, Issue 7
  • DOI: 10.1093/molbev/msw054

Infection by a Giant Virus (AaV) Induces Widespread Physiological Reprogramming in Aureococcus anophagefferens CCMP1984 – A Harmful Bloom Algae
journal, April 2018

  • Moniruzzaman, Mohammad; Gann, Eric R.; Wilhelm, Steven W.
  • Frontiers in Microbiology, Vol. 9
  • DOI: 10.3389/fmicb.2018.00752

The carbon balance of North American wetlands
journal, December 2006


Testing the cause of the Sphagnum austinii (Sull. ex Aust.) decline: Multiproxy evidence from a raised bog in Northern Ireland
journal, February 2015


Testing of null hypotheses in exploratory community analyses: similarity profiles and biota-environment linkage
journal, November 2008

  • Clarke, K. Robert; Somerfield, Paul J.; Gorley, Raymond N.
  • Journal of Experimental Marine Biology and Ecology, Vol. 366, Issue 1-2
  • DOI: 10.1016/j.jembe.2008.07.009

HMMER web server: 2015 update
journal, May 2015

  • Finn, Robert D.; Clements, Jody; Arndt, William
  • Nucleic Acids Research, Vol. 43, Issue W1
  • DOI: 10.1093/nar/gkv397

pplacer: linear time maximum-likelihood and Bayesian phylogenetic placement of sequences onto a fixed reference tree
journal, October 2010

  • Matsen, Frederick A.; Kodner, Robin B.; Armbrust, E. Virginia
  • BMC Bioinformatics, Vol. 11, Issue 1
  • DOI: 10.1186/1471-2105-11-538

The phylogeny of RNA-dependent RNA polymerases of positive-strand RNA viruses
journal, September 1991


Investigations of the structure and function of bacterial communities associated with Sphagnum mosses
journal, November 2007


Cell-wall polysaccharides play an important role in decay resistance of Sphagnum and actively depressed decomposition in vitro
journal, April 2010


How Sphagnum bogs down other plants
journal, July 1995