Top-Down Controls of Bacterial Metabolism: A Case Study from a Temperate Freshwater Lake Ecosystem

Abstract

In freshwater environments, limited data exist on the impact of mortality forces (viruses and heterotrophic nanoflagellates) on bacterial growth efficiency (BGE, index of bacterial carbon metabolism) compared to resource availability. An investigation to determine the relative influence of viral lysis and flagellate predation (top-down forces) on BGE was conducted in a mesotrophic freshwater system (Lake Goule, France) with time and space. Viral abundance was significantly (p < 0.001) related to bacterial abundance by a power law function with an exponent less than 1, emphasizing that the increases in host population (bacteria) together with viruses were not proportionate. A lytic viral strategy was evident throughout the study period, with high lysis of the bacterial population (up to 60%) supported by viral production rates. Viral processes (lysis and production) that were influenced by bacterial production and heterotrophic nanoflagellate abundance had a positive impact on BGE. Estimates of BGE were variable (9.9–45.5%) due to uncoupling between two metabolic parameters—namely bacterial production and respiration. The existence of a synergistic relationship between viruses and flagellates with bacteria in Lake Goule highlighted the decisive impact of top-down agents in sustaining the bacterial carbon metabolism of non-infected population through the nature of vital resources released via mortality processes.

Differential Effects of Viruses on the Growth Efficiency of Freshwater Bacterioplankton in Eutrophic Relative to Non-Eutrophic Lakes

“…In contrast to eutrophic, viral lysis yielded a significant positive relationship with BGE in the non-eutrophic lakes, which perhaps indicates that the nutrient spill as a consequence of host cell lysis could provide important substrates for the growth of certain bacterial groups during the period of nutrient limitation, similar to reports from freshwater systems [ 21 , 56 ]. In addition to viral lysis, protistan grazing activity can equally stimulate the growth of non-targeted bacterial communities through the supply of vital resources [ 57 ].…”

“…We carried out multiple correlation analyses to determine whether BGE was coupled to any of the physical, chemical, and biological variables available. Overall, the wide variability in the BGE (10–60%) in the studied systems was explained by the uncoupling between production and respiration, which confers advantageous to natural bacterioplankton in freshwater bodies [ 21 , 47 , 48 ] that are prone to fluctuating nutrient conditions caused by physical and climatic disturbances. Published reports on the factors influencing BGE in a particular system or set of systems have largely been attributed to their differences in nutrient concentration or availability [ 8 ].…”

“…Temperature, DOC, and chlorophyll concentration showed significant, positive covariation with bacterial parameters (abundance, production, and growth efficiency), suggesting bottom-up control of bacterial populations in the non-eutrophic lakes. However, high viral abundances accompanied by high viral infection together with a non-significant relationship of bacterial abundance with production and bottom-up forces (temperature, DOC, and chlorophyll) in eutrophic lakes lend support to a greater role and importance of viral lysis on BGE [ 18 , 20 , 21 , 49 ]: an issue that was previously raised in past studies [ 16 , 17 ]. We principally focused on lytic viruses, which through subsequent accelerated production of phage particles, directly contribute to viral shunt rather than dormant temperate viruses.…”

“…Viral regulation of bacterial metabolism is less well-studied than resource availability. Studies conducted so far have revealed contrasting and complex scenarios concerning the viral impact on BGE in marine [ 18 , 19 ] and freshwaters [ 20 , 21 ].…”