Succession of bacteria and archaea within the soil micro-food web

Abstract

Bacterivorous nematodes represent numerically abundant bacterial grazers in the soil micro-food web. Their trophic regulation shapes the soil microbiome, but the underlying population dynamics of bacteria and archaea are poorly understood. Here, we followed bulk soil respiration and time-resolved population dynamics (32 days) of bacterial and archaeal species in response to top-down control by a common bacterivorous soil nematode, Acrobeloides buetschlii, bottom-up control by resource amendment via maize litter as well as the combination of both. Addition of maize litter significantly increased soil respiration rates, while bacterivorous nematodes shifted the maximum rate of soil respiration from day 12 to day 6. Underlying bacterial and archaeal abundance changes could be separated into five major response types, dominating in different top-down and bottom-up control scenarios. Individual microbial species switched between response types depending on the different scenarios. In-depth analysis of these differential abundance patterns revealed a broad feeding behavior for A. buetschlii on dominating populations of gram-negative bacteria (Acidobacteriota, Bacteroidota, Gemmatimonatoda, Pseudomonadota) and ammonia-oxidizing archaea (Nitrososphaerota), while discriminating against dominant populations of gram-positive bacteria (Actinobacteriota, Bacillota). Combined bottom-up control by maize litter and top-down control by nematode grazing caused a succession of soil microbiota, which was driven by population changes first in the Bacteroidota, then in the Pseudomonadota, and last in the Acidobacteriota and Nitrososphaerota. This mechanistic understanding of nematode grazing on soil microbiota population dynamics is essential to inform predictive models of the soil food web.