Viral Induced Microbial Mortality in Arctic Hypersaline Spring Sediments.

Jesse Colangelo-Lillis,Boswell A Wing,Isabelle Raymond-Bouchard,Lyle G Whyte

doi:10.3389/fmicb.2016.02158

Abstract

Viruses are a primary influence on microbial mortality in the global ocean. The impacts of viruses on their microbial hosts in low-energy environments are poorly explored and are the focus of this study. To investigate the role of viruses in mediating mortality in low-energy environments where contacts between viruses and microbes are infrequent, we conducted a set of in situ time series incubations in the outlet and channel sediments of two cold, hypersaline springs of the Canadian High Arctic. We found microbial and viral populations in dynamic equilibrium, indicating approximately equal birth and death rates for each population. In situ rates of microbial growth were low (0.5–50 × 103 cells cm-3 h-1) as were rates of viral decay (0.09–170 × 104 virions cm-3 h-1). A large fraction of the springs’ viral communities (49–100%) were refractory to decay over the timescales of our experiments. Microcosms amended with lactate or acetate exhibited increased microbial growth rates (up to three-fold) indicating organic carbon as one limiting resource for the microbial communities in these environments. A substantial fraction (15–71%) of the microbial populations contained inducible proviruses that were released- occasionally in multiple pulses- over the eight monitored days following chemical induction. Our findings indicate that viruses in low-energy systems maintain low rates of production and activity, have a small but notable impact on microbial mortality (8–29% attenuation of growth) and that successful viral replication may primarily proceed by non-lethal strategies. In cold, low biomass marine systems of similar character (e.g., subsurface sediments), viruses may be a relatively minor driver of community mortality compared to less energy-limited environments such as the marine water column or surface sediments.

Highlights

Sunlight and photosynthesis are the drivers for surface life and environments sufficiently connected to utilize macromolecules synthesized in the photic zone
This work describes viral dynamics experiments performed in cold, oligotropic sediments of polar hypersaline spring sediments in the Canadian High Arctic in order to address two questions: (1) Is there is a direct relationship between trophic conditions and the predatory influence exerted by viruses on their microbial hosts? (2) Are viruses capable of lysogenic replication more common in oligotrophic environments? These questions form the basis for the trophic hypothesis of viral influence on microbial growth (Corinaldesi et al, 2003) and have implications for microbial ecology and evolution
Constant in situ abundances of microbes and viruses and dividing cells are consistent with microbial and viral abundances measured from the same spring sediments in summer of 2013 (Colangelo-Lillis et al, 2016b). These measurements suggest that microbial and viral populations in these sediments are each in dynamic equilibrium, both throughout our sampling period (July 11–18, 2015) and potentially across annual seasons (July; 2013 and 2015). This dynamic equilibrium indicates that endogenous rates of viral production and decay are balanced

Summary

Introduction

Sunlight and photosynthesis are the drivers for surface life and environments sufficiently connected to utilize macromolecules synthesized in the photic zone (e.g., marine surface sediments). In environments decoupled from photoautotrophy, the source of electron potential can limit microbial growth Examples of these environments include aquifers, subsurface lakes, glacial beds, permafrost environments, marine subsurface sediments, and any surface environment whose chemistry inhibits the growth of photosynthetic life (e.g., Don Juan pond; Siegel et al, 1979). Environments lacking in a substantial contribution of chemoautotrophic carbon fixation can be thought of as ‘low energy’ habitats, characterized by low biomass, low rates of microbial growth, and low rates of metabolism (Hoehler and Jørgensen, 2013). Microbes in these environments exhibit adaptation to low nutrient fluxes This work focuses on viral predation on microbes under low energy conditions

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