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

Ruth-Anne Sandaa,Aud Larsen,Birte Töpper,Selina Våge,Tron Thingstad,Bernadette Pree,Joachim Töpper,Runar Thyrhaug

doi:10.3390/v9090238

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.

Highlights

Microorganisms are the main controllers of biomass and energy fluxes in the ocean
A closed system will have a steady state with mineral nutrient-limited (MNL) bacterial growth at low ciliate abundances with a shift towards organic carbon limited (OCL) heterotrophic prokaryote growth at high ciliate abundances (Figure 1D)
Supplying allochthonous labile organic-C to an organic carbon limitation (OCL) system is expected to evoke a marked response, compared to no response when adding it to a system in the mineral nutrients (MNL) state

Summary

Introduction

Microorganisms are the main controllers of biomass and energy fluxes in the ocean Together with their viruses, they form a tightly linked web of trophic interactions at the base of marine food webs, typically connected to the higher part of the food chain with multicellular organisms through copepod predation on microbes. Within the microbial part of this ecosystem, the composition and activity of the community of pelagic heterotrophic prokaryotes are presumably shaped both by bottom-up factors such as the availability of mineral and organic-C nutrients, and by the top-down mechanisms of predation [1] and viral lysis [2,3,4]. Nutrient availability and predator control have to a large extent been studied using a “black box” approach, treating the heterotrophic prokaryotes as one plankton functional type (PFT), disregarding internal community composition and differences in activity between community members [5,6], and leaving us with a limited understanding of how population dynamics at the two levels of resolution are connected.

Methods

Results

Conclusion