Horizontal gene transfer-mediated bacterial strain variation affects host fitness in Drosophila

Abstract

Background How microbes affect host fitness and environmental adaptation has become a fundamental research question in evolutionary biology. To better understand the role of microbial genomic variation for host fitness, we tested for associations of bacterial genomic variation and Drosophila melanogaster offspring number in a microbial Genome Wide Association Study (GWAS). Results We performed a microbial GWAS, leveraging strain variation in the genus Gluconobacter, a genus of bacteria that are commonly associated with Drosophila under natural conditions. We pinpoint the thiamine biosynthesis pathway (TBP) as contributing to differences in fitness conferred to the fly host. While an effect of thiamine on fly development has been described, we show that strain variation in TBP between bacterial isolates from wild-caught D. melanogaster contributes to variation in offspring production by the host. By tracing the evolutionary history of TBP genes in Gluconobacter, we find that TBP genes were most likely lost and reacquired by horizontal gene transfer (HGT). Conclusion Our study emphasizes the importance of strain variation and highlights that HGT can add to microbiome flexibility and potentially to host adaptation.

Decoding host-microbiome interactions through co-expression network analysis within the non-human primate intestine

“…These studies highlight the fact that a single or a small number of host genes are controlling or are controlled by the intestinal microbiome. Conversely, a small number of microbiome genes can affect the host’s metabolic ( 53 ), fitness ( 54 ), and longevity ( 55 ) phenotypes. For example, structural mutations in the gene related to butyrate transport in Anaerostipes hadrus are strongly associated with a reduction in the host’s metabolic risk ( 53 ), and the intestinal microbiome’s thiamine biosynthesis genes, transferred by horizontal transmission, influence the host’s fitness ( 54 ).…”

“…Conversely, a small number of microbiome genes can affect the host’s metabolic ( 53 ), fitness ( 54 ), and longevity ( 55 ) phenotypes. For example, structural mutations in the gene related to butyrate transport in Anaerostipes hadrus are strongly associated with a reduction in the host’s metabolic risk ( 53 ), and the intestinal microbiome’s thiamine biosynthesis genes, transferred by horizontal transmission, influence the host’s fitness ( 54 ). Considering these previous studies and our results, it is suggested that the interaction between the host and the microbiome involves widespread influence of one’s genes on the activity of the other.…”