Title: Viral infections likely mediate microbial controls on ecosystem responses to global warming

Journal Article · · FEMS Microbiology Ecology (Online)

Abstract Climate change is affecting how energy and matter flow through ecosystems, thereby altering global carbon and nutrient cycles. Microorganisms play a fundamental role in carbon and nutrient cycling and are thus an integral link between ecosystems and climate. Here, we highlight a major black box hindering our ability to anticipate ecosystem climate responses: viral infections within complex microbial food webs. We show how understanding and predicting ecosystem responses to warming could be challenging—if not impossible—without accounting for the direct and indirect effects of viral infections on different microbes (bacteria, archaea, fungi, protists) that together perform diverse ecosystem functions. Importantly, understanding how rising temperatures associated with climate change influence viruses and virus-host dynamics is crucial to this task, yet is severely understudied. In this perspective, we (i) synthesize existing knowledge about virus-microbe-temperature interactions and (ii) identify important gaps to guide future investigations regarding how climate change might alter microbial food web effects on ecosystem functioning. To provide real-world context, we consider how these processes may operate in peatlands—globally significant carbon sinks that are threatened by climate change. We stress that understanding how warming affects biogeochemical cycles in any ecosystem hinges on disentangling complex interactions and temperature responses within microbial food webs.

Research Organization:
Duke University, Durham, NC (United States); Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)
Sponsoring Organization:
USDOE; USDOE Office of Science (SC), Biological and Environmental Research (BER)
Grant/Contract Number:
AC05-00OR22725; SC0020362
OSTI ID:
1959277
Journal Information:
FEMS Microbiology Ecology (Online), Journal Name: FEMS Microbiology Ecology (Online) Journal Issue: 3 Vol. 99; ISSN 1574-6941
Publisher:
Oxford University PressCopyright Statement
Country of Publication:
Netherlands
Language:
English

References (128)

Rapid loss of an ecosystem engineer: Sphagnum decline in an experimentally warmed bog journal October 2019
Parasite and pathogen effects on ecosystem processes: A quantitative review journal May 2020
Warming advances virus population dynamics in a temperate freshwater plankton community journal May 2020
Food Webs and Nutrient Cycling in Soils: Interactions and Positive Feedbacks book January 1996
Intraguild Predation: Predatory Networks at the Microbial Scale book January 2020
The Ecology of Sphagnum book January 1982
Seasonal Depth-Related Gradients in Virioplankton: Standing Stock and Relationships with Microbial Communities in Lake Pavin (France) journal May 2009
Contrasted Micro-Eukaryotic Diversity Associated with Sphagnum Mosses in Tropical, Subtropical and Temperate Climatic Zones journal February 2019
The Microbial Loop at the Surface of a Peatland:Structure, Function, and Impact of Nutrient Input journal January 1998
N2-fixation by methanotrophs sustains carbon and nitrogen accumulation in pristine peatlands journal August 2014
Ecological importance of soil bacterivores for ecosystem functions journal September 2015
Carbon Storage and Fluxes within Freshwater Wetlands: a Critical Review journal December 2009
The response of peatlands to climate warming: A review journal June 2011
Experimental warming and precipitation reduction affect the biomass of microbial communities in a Sphagnum peatland journal May 2020
Ecology of prokaryotic viruses journal May 2004
The microbial loop – 25 years later journal November 2008
Highly Diverse and Seasonally Dynamic Protist Community in a Pristine Peat Bog journal January 2011
Soil protistology rebooted: 30 fundamental questions to start with journal August 2017
Viruses in soil: Nano-scale undead drivers of microbial life, biogeochemical turnover and ecosystem functions journal December 2018
Trophic Regulations of the Soil Microbiome journal September 2019
Protists: Puppet Masters of the Rhizosphere Microbiome journal February 2019
Will changes in soil organic carbon act as a positive or negative feedback on global warming? journal January 2000
Global peatland dynamics since the Last Glacial Maximum: GLOBAL PEATLANDS SINCE THE LGM journal July 2010
Marine viruses and their biogeochemical and ecological effects journal June 1999
Environmental warming alters food-web structure and ecosystem function journal November 1999
Permafrost collapse is accelerating carbon release journal April 2019
A multitrophic model to quantify the effects of marine viruses on microbial food webs and ecosystem processes journal January 2015
Latitudinal variation in virus-induced mortality of phytoplankton across the North Atlantic Ocean journal August 2015
Temperature is a key factor in Micromonas–virus interactions journal January 2017
Viruses in the sea journal September 2005
Carbon respiration from subsurface peat accelerated by climate warming in the subarctic journal July 2009
Climate change and the permafrost carbon feedback journal April 2015
Microbial mediation of carbon-cycle feedbacks to climate warming journal December 2011
Microorganisms and climate change: terrestrial feedbacks and mitigation options journal October 2010
Protists as catalyzers of microbial litter breakdown and carbon cycling at different temperature regimes journal October 2020
Novel metabolic interactions and environmental conditions mediate the boreal peatmoss-cyanobacteria mutualism journal November 2021
Community-level respiration of prokaryotic microbes may rise with global warming journal November 2019
Cross-biome patterns in soil microbial respiration predictable from evolutionary theory on thermal adaptation journal January 2019
Phage puppet masters of the marine microbial realm journal June 2018
Host-linked soil viral ecology along a permafrost thaw gradient journal July 2018
Scientists’ warning to humanity: microorganisms and climate change journal June 2019
Towards an integrative view of virus phenotypes journal September 2021
Ecosystem warming extends vegetation activity but heightens vulnerability to cold temperatures journal August 2018
Effects of temperature and photosynthetically active radiation on virioplankton decay in the western Pacific Ocean journal January 2018
An unexpected role for mixotrophs in the response of peatland carbon cycling to climate warming journal November 2015
Scaling the metabolic balance of the oceans journal May 2006
Global warming benefits the small in aquatic ecosystems journal July 2009
Systematic variation in the temperature dependence of physiological and ecological traits journal May 2011
Methanotrophy induces nitrogen fixation during peatland development journal December 2013
The biomass distribution on Earth journal May 2018
Large stocks of peatland carbon and nitrogen are vulnerable to permafrost thaw journal August 2020
Linking species traits and demography to explain complex temperature responses across levels of organization journal October 2021
Homeoviscous Adaptation--A Homeostatic Process that Regulates the Viscosity of Membrane Lipids in Escherichia coli journal February 1974
The Relationship Between Bacterial Growth and Phage Production journal November 1937
The Growth of Bacteriophage journal January 1939
Critical Thermal Increment for the Movement of Oscillatoria journal September 1924
Climate Change Disequilibrium of Boreal Permafrost Peatlands Caused by Local Processes journal March 1998
Effects of Body Size and Temperature on Population Growth journal March 2004
Metabolic Theory and the Temperature-Size Rule Explain the Temperature Dependence of Population Carrying Capacity journal December 2018
Viruses of fungi and oomycetes in the soil environment journal July 2019
Soil protists: a fertile frontier in soil biology research journal February 2018
Evolving paradigms in biological carbon cycling in the ocean journal July 2018
Warming effects on marine microbial food web processes: how far can we go when it comes to predictions?
  • Sarmento, Hugo; Montoya, José M.; Vázquez-Domínguez, Evaristo
  • Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 365, Issue 1549 https://doi.org/10.1098/rstb.2010.0045
journal July 2010
Climate change in size-structured ecosystems journal November 2012
Novel communities from climate change journal November 2012
Linking community size structure and ecosystem functioning using metabolic theory journal November 2012
The Effect of Temperature on the Ecology of Aquatic Bacteriophages journal January 1980
Bacteriophage T4 Development Depends on the Physiology of its Host Escherichia Coli journal January 1997
Resilience of rhizosphere microbial predators and their prey communities after an extreme heat event journal October 2020
Temperature dependence of trophic interactions are driven by asymmetry of species responses and foraging strategy journal May 2013
Genetic and plastic rewiring of food webs under climate change journal June 2021
Global biogeochemical impacts of phytoplankton: a trait-based perspective journal October 2015
Desiccation and rehydration of mosses greatly increases resource fluxes that alter soil carbon and nitrogen cycling journal March 2019
Factors affecting virus dynamics and microbial host - virus interactions in marine environments journal May 2014
Viral ecology comes of age: Crystal ball journal February 2017
Big answers from small worlds: a user's guide for protist microcosms as a model system in ecology and evolution journal December 2014
Letter: Trophic interactions regulate peatland carbon cycling journal February 2021
Above- and belowground linkages in Sphagnum peatland: climate warming affects plant-microbial interactions journal December 2012
Bryophyte-cyanobacteria associations as regulators of the northern latitude carbon balance in response to global change journal March 2013
Crossing regimes of temperature dependence in animal movement journal February 2016
Experimental warming alters the community composition, diversity, and N 2 fixation activity of peat moss ( Sphagnum fallax ) microbiomes journal May 2019
Temporal variation in freshwater viral and bacterial community composition journal June 2008
Linking the global carbon cycle to individual metabolism journal April 2005
Parasites in food webs: the ultimate missing links: Parasites in food webs journal May 2008
Marine viruses and global climate change journal November 2011
Seasonal variations in the abundance of virus-like particles and bacteria in the floodwater of a Japanese paddy field journal August 2007
Ecology of viruses in soils: Past, present and future perspectives journal February 2008
The Sphagnum microbiome: new insights from an ancient plant lineage journal February 2016
Habitat‐adapted microbial communities mediate Sphagnum peatmoss resilience to warming journal March 2022
Primary Production of the Biosphere: Integrating Terrestrial and Oceanic Components journal July 1998
The Global Carbon Cycle: A Test of Our Knowledge of Earth as a System journal October 2000
Diversity of Active Viral Infections within the Sphagnum Microbiome journal September 2018
Environmental Transcription of mmoX by Methane-Oxidizing Proteobacteria in a Subarctic Palsa Peatland journal October 2012
Seasonal variations of virus abundance and viral control of the bacterial production in a backwater system of the danube river. journal January 1995
Effect of temperature on motility and chemotaxis of Escherichia coli journal September 1976
Effect of Temperature on the Composition of Fatty Acids in Escherichia coli journal January 1962
Soil Viruses Are Underexplored Players in Ecosystem Carbon Processing journal October 2018
Carbon cycling in peatlands — A review of processes and controls journal May 2002
Peatlands and Global Change: Response and Resilience journal November 2016
Zooplankton and the Ocean Carbon Cycle journal January 2017
Viruses in Soil Ecosystems: An Unknown Quantity Within an Unexplored Territory journal September 2017
Metabolic reprogramming by viruses in the sunlit and dark ocean journal January 2013
Minnesota peat viromes reveal terrestrial and aquatic niche partitioning for local and global viral populations journal November 2021
Warming and Resource Availability Shift Food Web Structure and Metabolism journal August 2009
Temperature-Induced Viral Resistance in Emiliania huxleyi (Prymnesiophyceae) journal November 2014
Molecular prediction of lytic vs lysogenic states for Microcystis phage: Metatranscriptomic evidence of lysogeny during large bloom events journal September 2017
Toward a Metabolic Theory of Ecology journal July 2004
Viruses and Nutrient Cycles in the Sea journal October 1999
Northern Peatlands: Role in the Carbon Cycle and Probable Responses to Climatic Warming journal May 1991
Effect of temperature on the algicidal activity and the stability of HaV (Heterosigma akashiwo virus) journal January 1998
Temperature alters algicidal activity of DNA and RNA viruses infecting Chaetoceros tenuissimus journal October 2014
Effects of temperature, salinity and clay particles on inactivation and decay of cold-active marine Bacteriophage 9A journal October 2006
The Ecological Role of Water-Column Microbes in the Sea journal January 1983
Viral dynamics: a model of the effects of size shape, motion and abundance of single-celled olanktonic organisms and other particles journal January 1992
Microbial control over carbon cycling in soil journal January 2012
Temperature dependent bacteriophages of a tropical bacterial pathogen journal November 2014
Diversity and comparative genomics of Microviridae in Sphagnum- dominated peatlands journal April 2015
Dynamics of Viral Abundance and Diversity in a Sphagnum-Dominated Peatland: Temporal Fluctuations Prevail Over Habitat journal January 2016
Editorial: Anthropogenic Impacts on the Microbial Ecology and Function of Aquatic Environments journal July 2016
Warming and CO2 Enhance Arctic Heterotrophic Microbial Activity journal March 2019
Temporal Dynamics of Soil Virus and Bacterial Populations in Agricultural and Early Plant Successional Soils journal July 2020
Episodic Decrease in Temperature Increases mcy Gene Transcription and Cellular Microcystin in Continuous Cultures of Microcystis aeruginosa PCC 7806 journal December 2020
Protist Predation Influences the Temperature Response of Bacterial Communities journal April 2022
Influence of Irradiance and Temperature on the Virus MpoV-45T Infecting the Arctic Picophytoplankter Micromonas polaris journal November 2018
Characterization and Temperature Dependence of Arctic Micromonas polaris Viruses journal June 2017
Role of microbes in pelagic food webs: A revised concept journal September 1988
The role of sunlight in the removal and repair of viruses in the sea journal June 1998
Temperature alters the shape of predator–prey cycles through effects on underlying mechanisms journal January 2020