Structured foraging of soil predators unveils functional responses to bacterial defenses
Fernando W. Rossine, Gabriel Vercelli, Corina Tarnita, and Thomas Gregor. Proceedings of the National Academy of Science (USA) 119(52): e2210995119 (2022).
Abstract
Predators and their foraging strategies often determine ecosystem structure and function. Yet, the role of protozoan predators in microbial soil ecosystems remains elusive despite the importance of these ecosystems to global biogeochemical cycles. In particular, amoebae — the most abundant soil protozoan predator of bacteria — remineralize soil nutrients and shape the bacterial community. However, their foraging strategies and their role as microbial ecosystem engineers remain unknown. Here we present a multi-scale approach, connecting microscopic single-cell analysis and macroscopic whole ecosystem dynamics, to expose a phylogenetically widespread foraging strategy, in which an amoeba population spontaneously partitions between cells with fast, polarized movement and cells with slow, unpolarized movement. Such differentiated motion gives rise to efficient colony expansion and consumption of the bacterial substrate. From these insights, we construct a theoretical model that predicts how disturbances to amoeba growth rate and movement disrupt their predation efficiency. These disturbances correspond to distinct classes of bacterial defenses, which allows us to experimentally validate our predictions. All considered, our characterization of amoeba foraging identifies amoeba mobility, and not amoeba growth, as the core determinant of predation efficiency and a key target for bacterial defense systems.
Significance Statement
Characterization of foraging strategies is crucial to a predictive and mechanistic understanding of the impact that soil protozoan predators—of which amoebae are the most abundant—have on microbial community composition and dynamics. We show that a clonal population of soil amoebae invading a spatially structured bacterial matrix spontaneously differentiates into subpopulations with different types of movement. This strategy determines both the rates of bacteria consumption and the effectiveness of different bacterial anti-predator defenses. We further show that such cell behavior differentiation and coordinated movement are conserved, ancestral features of amoebozoans. Since differentiation and coordination are necessary elements of multicellular development, our results suggest that unicellular foraging strategies could have facilitated the multiple independent origins of multicellularity across soil amoebae.