Diversity of Active Viral Infections within the Sphagnum Microbiome
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 Sphagnum peat 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 »
- Authors:
-
- Univ. of Tennessee, Knoxville, TN (United States)
- Georgia Inst. of Technology, Atlanta, GA (United States)
- Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
- Univ. of Illinois at Urbana-Champaign, Urbana, IL (United States)
- Publication Date:
- Research Org.:
- Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)
- Sponsoring Org.:
- USDOE
- OSTI Identifier:
- 1482449
- Grant/Contract Number:
- AC05-00OR22725
- Resource Type:
- Accepted Manuscript
- 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. https://doi.org/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. https://doi.org/10.1128/AEM.01124-18. https://www.osti.gov/servlets/purl/1482449.
@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 = {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 Sphagnum peat 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. 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. 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},
number = 23,
volume = 84,
place = {United States},
year = {Thu Nov 15 00:00:00 EST 2018},
month = {Thu Nov 15 00:00:00 EST 2018}
}
Web of Science
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
- Mellegård, H.; Stalheim, T.; Hormazabal, V.
- Letters in Applied Microbiology, Vol. 49, Issue 1
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
The ecological significance of organochemical compounds in Sphagnum
journal, June 1997
- Verhoeven, J. T. A.; Liefveld, W. M.
- Acta Botanica Neerlandica, Vol. 46, Issue 2
Metagenomics and biodiversity of sphagnum bogs
journal, September 2016
- Rusin, L. Yu.
- Molecular Biology, Vol. 50, Issue 5
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
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
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
Soil carbon pools and world life zones
journal, July 1982
- Post, Wilfred M.; Emanuel, William R.; Zinke, Paul J.
- Nature, Vol. 298, Issue 5870
Cyanophage Diversity, Inferred from g20 Gene Analyses, in the Largest Natural Lake in France, Lake Bourget
journal, February 2004
- Dorigo, U.; Jacquet, S.; Humbert, J. -F.
- Applied and Environmental Microbiology, Vol. 70, Issue 2
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
Formation, succession and landscape history of Central-European summit raised bogs: A multiproxy study from the Hrubý Jeseník Mountains
journal, August 2012
- Dudová, Lydie; Hájková, Petra; Buchtová, Hana
- The Holocene, Vol. 23, Issue 2
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
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
Virus taxonomy in the age of metagenomics
journal, January 2017
- Simmonds, Peter; Adams, Mike J.; Benkő, Mária
- Nature Reviews Microbiology, Vol. 15, Issue 3
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
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
Northern Peatlands: Role in the Carbon Cycle and Probable Responses to Climatic Warming
journal, May 1991
- Gorham, Eville
- Ecological Applications, Vol. 1, Issue 2
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
The Role of Bryophytes in Carbon and Nitrogen Cycling
journal, September 2003
- Turetsky, Merritt R.
- The Bryologist, Vol. 106, Issue 3
Natural nitrogen filter fails in polluted raised bogs
journal, June 2000
- Lamers, Leon P. M.; Bobbink, Roland; Roelofs, Jan G. M.
- Global Change Biology, Vol. 6, Issue 5
Nitrogen fixation in Sphagnum mosses is affected by moss species and water table level
journal, December 2014
- Leppänen, Sanna M.; Rissanen, Antti J.; Tiirola, Marja
- Plant and Soil, Vol. 389, Issue 1-2
Similar Diversity of Alphaproteobacteria and Nitrogenase Gene Amplicons on Two Related Sphagnum Mosses
journal, January 2012
- Bragina, Anastasia; Maier, Stefanie; Berg, Christian
- Frontiers in Microbiology, Vol. 2
Resilience of plant and testate amoeba communities after climatic and anthropogenic disturbances in a Baltic bog in Northern Poland: Implications for ecological restoration
journal, July 2016
- Gałka, Mariusz; Tobolski, Kazimierz; Górska, Aleksandra
- The Holocene, Vol. 27, Issue 1
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
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
Standing on the Shoulders of Giant Viruses: Five Lessons Learned about Large Viruses Infecting Small Eukaryotes and the Opportunities They Create
journal, August 2016
- Wilhelm, Steven W.; Coy, Samantha R.; Gann, Eric R.
- PLOS Pathogens, Vol. 12, Issue 8
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
Assessing the Diversity and Specificity of Two Freshwater Viral Communities through Metagenomics
journal, March 2012
- Roux, Simon; Enault, Francois; Robin, Agnès
- PLoS ONE, Vol. 7, Issue 3
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
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
The “Giant Virus Finder” discovers an abundance of giant viruses in the Antarctic dry valleys
journal, February 2017
- Kerepesi, Csaba; Grolmusz, Vince
- Archives of Virology, Vol. 162, Issue 6
Diversity and comparative genomics of Microviridae in Sphagnum- dominated peatlands
journal, April 2015
- Quaiser, Achim; Dufresne, Alexis; Ballaud, Flore
- Frontiers in Microbiology, Vol. 6
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
The resilience and functional role of moss in boreal and arctic ecosystems: Tansley review
journal, August 2012
- Turetsky, M. R.; Bond-Lamberty, B.; Euskirchen, E.
- New Phytologist, Vol. 196, Issue 1
Diversity and Antagonistic Potential of Bacteria Associated with Bryophytes from Nutrient-Poor Habitats of the Baltic Sea Coast
journal, November 2004
- Opelt, K.; Berg, G.
- Applied and Environmental Microbiology, Vol. 70, Issue 11
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
Flow cytometric detection and enumeration of DNA and RNA viruses infecting marine eukaryotic microalgae
journal, April 2007
- Tomaru, Yuji; Nagasaki, Keizo
- Journal of Oceanography, Vol. 63, Issue 2
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
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
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
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
IBS: an illustrator for the presentation and visualization of biological sequences: Fig. 1.
journal, June 2015
- Liu, Wenzhong; Xie, Yubin; Ma, Jiyong
- Bioinformatics, Vol. 31, Issue 20
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
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
Giant viruses with an expanded complement of translation system components
journal, April 2017
- Schulz, Frederik; Yutin, Natalya; Ivanova, Natalia N.
- Science, Vol. 356, Issue 6333
SortMeRNA: fast and accurate filtering of ribosomal RNAs in metatranscriptomic data
journal, October 2012
- Kopylova, Evguenia; Noé, Laurent; Touzet, Hélène
- Bioinformatics, Vol. 28, Issue 24
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
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
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
Genome of brown tide virus (AaV), the little giant of the Megaviridae, elucidates NCLDV genome expansion and host–virus coevolution
journal, October 2014
- Moniruzzaman, Mohammad; LeCleir, Gary R.; Brown, Christopher M.
- Virology, Vol. 466-467
An enzymic 'latch' on a global carbon store
journal, January 2001
- Freeman, Chris; Ostle, Nick; Kang, Hojeong
- Nature, Vol. 409, Issue 6817
Cytoscape: A Software Environment for Integrated Models of Biomolecular Interaction Networks
journal, November 2003
- Shannon, P.
- Genome Research, Vol. 13, Issue 11
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
Viruses and Nutrient Cycles in the Sea
journal, October 1999
- Wilhelm, Steven W.; Suttle, Curtis A.
- BioScience, Vol. 49, Issue 10
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
MUSCLE: a multiple sequence alignment method with reduced time and space complexity
journal, August 2004
- Edgar, Robert C.
- BMC Bioinformatics, Vol. 5, Issue 1, p. 113
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
Testing the cause of the Sphagnum austinii (Sull. ex Aust.) decline: Multiproxy evidence from a raised bog in Northern Ireland
journal, February 2015
- Swindles, Graeme T.; Turner, T. Edward; Roe, Helen M.
- Review of Palaeobotany and Palynology, Vol. 213
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
HMMER web server: 2015 update
journal, May 2015
- Finn, Robert D.; Clements, Jody; Arndt, William
- Nucleic Acids Research, Vol. 43, Issue W1
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
The phylogeny of RNA-dependent RNA polymerases of positive-strand RNA viruses
journal, September 1991
- Koonin, E. V.
- Journal of General Virology, Vol. 72, Issue 9
Sphagnan - a pectin-like polymer isolated from Sphagnum moss can inhibit the growth of some typical food spoilage and food poisoning bacteria by lowering the pH
journal, March 2009
- Stalheim, T.; Ballance, S.; Christensen, B. E.
- Journal of Applied Microbiology, Vol. 106, Issue 3
Investigations of the structure and function of bacterial communities associated with Sphagnum mosses
journal, November 2007
- Opelt, Katja; Chobot, Vladimir; Hadacek, Franz
- Environmental Microbiology, Vol. 9, Issue 11
Cell-wall polysaccharides play an important role in decay resistance of Sphagnum and actively depressed decomposition in vitro
journal, April 2010
- Hájek, Tomáš; Ballance, Simon; Limpens, Juul
- Biogeochemistry, Vol. 103, Issue 1-3
Evolution of eukaryotic single-stranded DNA viruses of the Bidnaviridae family from genes of four other groups of widely different viruses
journal, June 2014
- Krupovic, Mart; Koonin, Eugene V.
- Scientific Reports, Vol. 4, Issue 1
How Sphagnum bogs down other plants
journal, July 1995
- van Breemen, Nico
- Trends in Ecology & Evolution, Vol. 10, Issue 7
The carbon balance of North American wetlands
journal, December 2006
- Bridgham, Scott D.; Megonigal, J. Patrick; Keller, Jason K.
- Wetlands, Vol. 26, Issue 4
How Sphagnum bogs down other plants
journal, July 1995
- van Breemen, N.
- Trends in Ecology & Evolution, Vol. 10, Issue 7
Virus-host relationships of marine single-celled eukaryotes resolved from metatranscriptomics
text, January 2017
- Moniruzzaman, Mohammad; Wurch, Louie L.; Alexander, Harriet
- Columbia University
Viruses infecting a warm water picoeukaryote shed light on spatial co-occurrence dynamics of marine viruses and their hosts
journal, May 2021
- Bachy, Charles; Yung, Charmaine C. M.; Needham, David M.
- The ISME Journal
A sand fly salivary protein acts as a neutrophil chemoattractant
journal, May 2021
- Guimaraes-Costa, Anderson B.; Shannon, John P.; Waclawiak, Ingrid
- Nature Communications, Vol. 12, Issue 1
An SHR–SCR module specifies legume cortical cell fate to enable nodulation
journal, December 2020
- Dong, Wentao; Zhu, Yayun; Chang, Huizhong
- Nature, Vol. 589, Issue 7843
Метагеномика и биоразнообразие сфагновых болот
journal, January 2016
- Русин, Л. Ю.
- Молекулярная биология, Vol. 50, Issue 5
New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0
text, January 2010
- Guindon, Stéphane; Dufayard, Jean-François; Lefort, Vincent
- Oxford University Press
Correction: Dietary Essential Amino Acids Affect the Reproduction of the Keystone Herbivore Daphnia pulex
journal, June 2012
- Fink, Patrick; Pflitsch, Claudia; Marin, Kay
- PLoS ONE, Vol. 7, Issue 6
New Algorithms and Methods to Estimate Maximum-Likelihood Phylogenies: Assessing the Performance of PhyML 3.0
text, January 2010
- Guindon, Stéphane; Dufayard, Jean-François; Lefort, Vincent
- ETH Zurich
pplacer: linear time maximum-likelihood and Bayesian phylogenetic placement of sequences onto a fixed reference tree
preprint, January 2010
- Matsen, Frederick A.; Kodner, Robin B.; Armbrust, E. Virginia
- arXiv
Works referencing / citing this record:
Diel cycling of the cosmopolitan abundant Pelagibacter virus 37‐F6: one of the most abundant viruses on earth
journal, February 2020
- Martinez‐Hernandez, Francisco; Luo, Elaine; Tominaga, Kento
- Environmental Microbiology Reports, Vol. 12, Issue 2