Diet and Genotype of an Aquatic Invertebrate Affect the Composition of Free-Living Microbial Communities

Abstract

In spite of the growing interest in the role of the gut microbiome (GM) in host physiology and health, the mechanisms governing its assembly and its effects on the environment are poorly understood. In this article, we show that the host genotype and the GM of Daphnia influence the community structure of the surrounding bacterioplankton (BPK). When Daphnia genotypes were placed in an identical environment, both the GM and BPK showed a genotype and diet-dependent taxonomic composition. Overall, the GM strongly differed from the BPK in taxonomic composition and was characterized by a lower α-diversity, suggesting a selective rejecting of bacteria from the regional species pool. In a microbiome transplant experiment, the assembly of both the GM and BPK was strongly affected by the host genotype and the inoculum to which germ-free Daphnia were exposed. The combination of these results suggests a strong interaction between the host genotype, its GM and free-living microbial communities. Currently, it is generally assumed that an animal's diet has a strong effect on the animal's GM, but only a negligible (if any) effect on the surrounding environment. However, our results indicate that the diet/microbiome inocula have a small effect on the gut community and a large effect on the community in the surrounding environment. This structuring genotype × microbiome × environment effect is an essential prerequisite that could indicate that microbiomes play an important role in eco-evolutionary processes.

The bacterioplankton community composition and a host genotype dependent occurrence of taxa shape the Daphnia magna gut bacterial community

“… 2017a , Sullam et al . 2018 ; 2020 ; Sison-Mangus, Metzger and Ebert 2018 ; Frankel-Bricker et al . 2019 ; Mushegian et al .…”

“…Although the gut bacterial community was strongly influenced by the bacterial community in the medium, it was also clearly differentiated from it, a finding that is in agreement with previous studies (Freese and Schink 2011 ; Macke et al . 2017, 2020 ). All gut bacterial communities showed a higher degree of resemblance to each other than to any of the bacterial communities in media inoculated with natural bacterioplankton.…”

“…We consistently re-inoculated the medium with these bacterioplankton communities throughout the experiment to prevent strong modifications of the bacterioplankton community through selective lab conditions or impacts by Daphnia (Macke et al . 2020 ). This enables us to disentangle the effect of environmental bacteria, as a source of taxa from which gut bacterial communities are assembled, and host genotype on the Daphnia gut bacterial community composition under controlled conditions while mimicking more diverse and natural settings.…”

A methodological framework to analyse determinants of host–microbiota networks, with an application to the relationships between Daphnia magna's gut microbiota and bacterioplankton

“…The methodological framework we propose was successfully applied to results of an experiment aimed at uncovering the potential reciprocal effects of Daphnia gut microbiota and bacterioplankton in the face of diets of heterogeneous edibility. In an earlier study (Macke et al, 2020), we suggested that the gut microbiome was different from the surrounding bacterioplankton and that both microbial pools showed a dependency on Daphnia genotype and diet, on the basis of statistical analyses (GLM, PERMANOVA, Mantel tests) performed directly on the taxonomic composition and relative abundances of microbial samples. The present study confirms the difference between the two sample types (Figs.…”

“…The methods presented here were applied to experimental data obtained for another study (Macke et al, 2020).…”