The Response of Heterotrophic Prokaryote and Viral Communities to Labile Organic Carbon Inputs Is Controlled by the Predator Food Chain Structure

Abstract

Factors controlling the community composition of marine heterotrophic prokaryotes include organic-C, mineral nutrients, predation, and viral lysis. Two mesocosm experiments, performed at an Arctic location and bottom-up manipulated with organic-C, had very different results in community composition for both prokaryotes and viruses. Previously, we showed how a simple mathematical model could reproduce food web level dynamics observed in these mesocosms, demonstrating strong top-down control through the predator chain from copepods via ciliates and heterotrophic nanoflagellates. Here, we use a steady-state analysis to connect ciliate biomass to bacterial carbon demand. This gives a coupling of top-down and bottom-up factors whereby low initial densities of ciliates are associated with mineral nutrient-limited heterotrophic prokaryotes that do not respond to external supply of labile organic-C. In contrast, high initial densities of ciliates give carbon-limited growth and high responsiveness to organic-C. The differences observed in ciliate abundance, and in prokaryote abundance and community composition in the two experiments were in accordance with these predictions. Responsiveness in the viral community followed a pattern similar to that of prokaryotes. Our study provides a unique link between the structure of the predator chain in the microbial food web and viral abundance and diversity.

Simple models combining competition, defence and resource availability have broad implications in pelagic microbial food webs

“…5b) was explained as the lack of effects from adding glucose to a system already replete in labile organic substrates. This as opposed to the low-copepod (high ciliate) situation favouring C-limited conditions and strong observed community responses to the glucose treatments (Sandaa et al 2017).…”

“…) responded, under comparable experimental perturbations, differently at the level of bacterial and viral community composition (Sandaa et al . ). In analogy with the Mediterranean case, this was interpreted using the simple pentagon of Fig.…”

“…This as opposed to the low‐copepod (high ciliate) situation favouring C‐limited conditions and strong observed community responses to the glucose treatments (Sandaa et al . ).…”

“…An experimental illustration of this is how the two Arctic mesocosm experiments with food web structures as represented in Fig. 4b and c (Larsen et al 2015) responded, under comparable experimental perturbations, differently at the level of bacterial and viral community composition (Sandaa et al 2017). In analogy with the Mediterranean case, this was interpreted using the simple pentagon of Fig.…”

Copepods promote bacterial community changes in surrounding seawater through farming and nutrient enrichment

“…These results represent bacterial abundances arising from the presence of copepods, with potential loss due to nanoflagellate grazing not considered. Although not measured, potential differences of the influence of nanoplankton among treatments could have contributed to some of the observed differences (Zollner et al, 2009;Sandaa et al, 2017). Zoosphere bacteria supported by copepods in nature likely recruit nanoflagellates, which in turn recruit microzooplankton that the copepods may feed on.…”