Infection paradox: high abundance but low impact of freshwater benthic viruses

Abstract

The discovery of an abundant and diverse virus community in oceans and lakes has profoundly reshaped ideas about global carbon and nutrient fluxes, food web dynamics, and maintenance of microbial biodiversity. These roles are exerted through massive viral impact on the population dynamics of heterotrophic bacterioplankton and primary producers. We took advantage of a shallow wetland system with contrasting microhabitats in close proximity to demonstrate that in marked contrast to pelagic systems, viral infection, determined directly by transmission electron microscopy, and consequently mortality of prokaryotes were surprisingly low in benthic habitats in all seasons. This was true even though free viruses were abundant throughout the year and bacterial infection and mortality rates were high in surrounding water. The habitats in which we found this pattern include sediment, decomposing plant litter, and biofilms on aquatic vegetation. Overall, we detected viruses in only 4 of a total of approximately 15,000 bacterial cells inspected in these three habitats; for comparison, nearly 300 of approximately 5,000 cells suspended in the water column were infected. The strikingly low incidence of impact of phages in the benthos may have important implications, since a major portion of microbial biodiversity and global carbon and nutrient turnover are associated with surfaces. Therefore, if failure to infect benthic bacteria is a widespread phenomenon, then the global role of viruses in controlling microbial diversity, food web dynamics, and biogeochemical cycles would be greatly diminished compared to predictions based on data from planktonic environments.

FIG. 1.

Seasonal changes in the abundance of free virus-like particles (VLPs) and ratios of viruses to bacteria (VBRs) in four microhabitats of a littoral freshwater marsh. (A and E) Marsh water column. (B and F) Biofilm on reed stems. (C and G) Decaying plant litter. (D and H) Aerobic top sediment layer. Error bars depict ±1 SE; n = 6 (each histogram).

FIG. 2.

Seasonal changes in parameters characterizing virus-bacterium interactions in the water column of a freshwater marsh. (A) FIC. (B) VIM. (C) Number of mature viruses per bacterial cell (burst size). (D) Virus production rate (per milliliter of water per day). Error bars depict ±1 SE; n = 6 (each histogram).