Implication of Viral Infections for Greenhouse Gas Dynamics in Freshwater Wetlands: Challenges and Perspectives

Abstract

Viruses are non-living, acellular entities, and the most abundant biological agents on earth. They are widely acknowledged as having the capacity to influence global biogeochemical cycles by infecting the bacterial and archaeal populations that regulate carbon and nutrient turnover. Evidence suggests that the majority of viruses in wetlands are bacteriophages, but despite their importance, studies on how viruses control the prokaryotic community and the concomitant impacts on ecosystem function (such as carbon cycling and greenhouse gas flux) in wetlands are rare. Here we investigate virus-prokaryote interactions in freshwater wetland ecosystems in the context of their potential influence on biogeochemical cycling. Specifically, we (1) synthesize existing literature to establish current understanding of virus-prokaryote interactions, focusing on the implications for wetland greenhouse gas dynamics and (2) identify future research priorities. Viral dynamics in freshwater wetlands have received much less attention compared to those in marine ecosystems. However, based on our literature review, within the last 10 years, viral ecology studies on freshwater wetlands have increased twofold. Despite this increase in literature, the potential implication of viral infections on greenhouse gas emission dynamics is still a knowledge gap. We hypothesize that the rate of greenhouse gas emissions and the pool of sequestered carbon could be strongly linked to the type and rate of viral infection. Viral replication mechanism choice will consequently influence the microbial efficiency of organic matter assimilation and thus the ultimate fate of carbon as a greenhouse gas or stored in soils.

Keywords: biogeochemical cycles; carbon dioxide; freshwater; infection; methane; prokaryote; virus; wetland.

Figure 1

Schematic representation of how different viral replication mechanisms might influence the microbial growth efficiency (MGE) and, consequently, the pool of sequestered carbon and the emissions of greenhouse gas. The lysogenic cycle affects prokaryotic metabolism by decreasing the organic matter usage and thus reducing the carbon decomposition. The lytic cycle affects the carbon turnover by recycling the organic matter already assimilated by prokaryotes and thus increasing the labile carbon available for decomposition. (Vectors used under license from Shutterstock.com).

Figure 2

Conceptual model outlining the hypothesized viral infection and organic matter dynamics when in transition from wet-to-dry and dry-to-wet conditions. (A) In the water column, the lytic cycle is recognized as the dominant infection strategy. The viral shunt results in the release of DOC that can be directly decomposed by microbes (1) or might coagulate into sinking aggregates (2). However, the high decomposition activities of the microbiota that colonize the sinking aggregates likely degrade the aggregates, leading to the production of GHG (3). The macromolecules released after the viral lysis can be recalcitrant and bypass microbial consumption. These compounds can reach the soil surface, along with labile organic matter escaping microbial attack within the sinking aggregates (4). (B) During a wet-to-dry transition, the reduction of the water column and the soil-water interface also reduces the diffusion of labile carbon organic matter (LOM) and extracellular hydrolytic enzymes (EHEs) across the water-soil interface (5), leading to increased remineralization of labile matter within the aerobic layer of the soil. Changes in physiochemical conditions triggered by the occurrence of wet-to-dry cycles can also facilitate the transformation of labile carbon into a stable form through the interaction with mineral soil (6). During dry-to-wet transitions, e.g. flooding events, the breakdown of soil aggregates and presence of the porewater matrix promotes virus-host encounters and the shift from soil-like to water-like viruses (7). This shift could affect the direction of carbon flow, possibly increasing GHG emissions (8). (C) In the soil, the fate of LOM can undergo two pathways: (9) microbial decomposition through aerobic or anaerobic reactions, (10) transformation into soil aggregates via physical or chemical reactions with mineral soil, i.e., transformation into recalcitrant organic matter (ROM). The promotion of viral infections and lysogeny through aggregate formation has been hypothesized as the dominant infection mechanism in soil. (Vectors used under license from Shutterstock.com).

Figure 3

Shifts in abiotic conditions have the potential to enact changes in the viral infection strategy and prokaryotic MGE. The microbial growth efficiency (MGE) defines the proportion of DOC that is being assimilated and then re-synthetized or re-respired with subsequent consequences on the production of carbon emissions. (Vectors used under license from Shutterstock.com).