Multi-scale ecological filters shape the crayfish microbiome

Abstract

A general and practical understanding of the processes that drive microbiome assembly and structure are paramount to understanding organismal biology, health, and evolution. In this study of stream-dwelling crayfish, we conceptualized colonization of microbial symbionts as a series of ecological filters that operate at the environment, host, and host microsite levels, and identified key ecological processes at each level. A survey of Cambarus sciotensis in western Virginia, USA, showed that the local environment and host microsites interact to create complex patterns of microbial diversity and composition. An in situ experiment confirmed a prevailing effect of host microsite on microbial composition, and also showed that an ectosymbiotic worm (Annelida; Branchiobdellida) which feeds on biofilms and other symbionts had significant effects on microbial composition of the host carapace, but not gills. Bacterial communities of the carapace were taxonomically rich and even, and correlated with microbial communities of the ambient environment. Conversely, communities on gills were less diverse and dominated by two taxa with potential functional significance: Comamonadaceae and Chitinophagaceae. The bacterial communities of the gills appear to be tightly coupled to host biology, and those of the carapace are mostly determined by environmental context. Our work provides the first characterization of the crayfish microbiome and shows how multi-scale and experimental studies of symbiont community assembly provide valuable insights into how the animal microbiome is structured under conditions of natural complexity. Furthermore, this study demonstrates that metazoan symbiont taxa, i.e., the branchiobdellidans, can alter microbiome assembly and structure.