A Generalist Protist Predator Enables Coexistence in Multitrophic Predator-Prey Systems Containing a Phage and the Bacterial Predator Bdellovibrio

Julia Johnke,Hauke Harms,Edouard Jurkevitch,Antonis Chatzinotas,Ariel Kushmaro,Maayan Baron,Marina De Leeuw

doi:10.3389/fevo.2017.00124

Abstract

Complex ecosystems harbor multiple predator and prey species whose direct and indirect interactions are understudied. In particular, the combined effects of predator diversity and resource preference on prey removal are not known. To better understand the effect of interspecies interactions combinations of micro-predators – i.e. protists (generalists), predatory bacteria (semi-specialists), and phages (specialists) – and bacterial prey were tracked over a 72-hour period in miniature membrane bioreactors. While specialist predators alone drove their preferred prey to extinction, the inclusion of a generalist resulted in uniform losses among prey species. Most importantly, presence of a generalist predator enabled coexistence of all predators and prey. As the generalist predator also negatively affected the other predators we suggest that resource partitioning between predators and the constant availability of resources for bacterial growth due to protist predation stabilizes the system and keeps its diversity high. The appearance of resistant prey strains and subsequent evolution of specialist predators unable to infect the ancestral prey implies that multitrophic communities are able to persist and stabilize themselves. Interestingly, the appearance of BALOs and phages unable to infect their prey was only observed for the BALO or phage in the absence of additional predators or prey species indicating that competition between predators might influence coevolutionary dynamics.

Highlights

Predatory interactions among organisms of different trophic levels are key processes that determine the coexistence in ecological communities
Three different micro-predators and three bacterial species were used in the study: a ciliate protist (Tetrahymena pyriformis), a Bdellovibrio and like organisms (BALOs) (B. bacteriovorus strain 109J), and a Klebsiella phage originally isolated from a wastewater treatment plant (WWTP) in Langenreichenbach, Germany
The micro-predators are characterized by different prey ranges: while the protist feeds on all three prey species, the BALO only preys upon the two Gramnegative bacteria (Klebsiella sp. and P. putida), and the phage infects only the Klebsiella strain (Figure 1)

Summary

Introduction

Predatory interactions among organisms of different trophic levels are key processes that determine the coexistence in ecological communities. Species-specific traits, such as resource specialization, strongly affected prey biomass and diversity (Jiang and Morin, 2005; Filip et al, 2014) and induced shifts in trophic cascades (Steiner, 2001). Studies focusing on the combined effect of multiple predators with different resource utilization are rare (Jiang and Morin, 2005; Diehl et al, 2013), but most likely better reflect natural communities and enable the direct observation of a major mediator of coexistence: resource partitioning (Chesson, 1991). Species not directly involved in consumptive interactions are the key to survival of susceptible prey and increased persistence of prey species in more complex food webs (Hammill et al, 2015)

Methods

Results

Conclusion