Simultaneous Single-Cell Genome and Transcriptome Sequencing of Termite Hindgut Protists Reveals Metabolic and Evolutionary Traits of Their Endosymbionts

Abstract

Different protist species which colonize the hindguts of wood feeding Reticulitermes termites are associated with endosymbiotic bacteria belonging to the genus Endomicrobium. In this study, we focused on the endosymbionts of three protist species from Reticulitermes flavipes, which included Pyrsonympha vertens, Trichonympha agilis, and Dinenympha species II. Since these protist hosts represented members of difference taxa which colonize different niches within the hindguts of their termite hosts, we investigated if these differences translated to differential gene content and expression in their endosymbionts. Following assembly and comparative genome and transcriptome analyses, we discovered that these endosymbionts differed with respect to possible niche specific traits such carbon metabolism. Our analyses supported that genes related to carbon metabolism were acquired by horizontal gene transfer (HGT) from donor taxa which are present in termites hindgut community. In addition, our analyses supported that these endosymbionts have retained and expressed genes related to natural transformation (competence) and recombination. Taken together, the presence of genes acquired by HGT and a putative competence pathway supported that these endosymbionts are not cut-off from gene flow and that competence may be a mechanism by which members of the Endomicrobium can acquire new traits. ImportanceThe composition and structure of wood, which contains cellulose, hemicellulose and lignin, prevents most organisms from using this common food source. Termites are a rare exception among animals, and they rely on a complex microbiome housed in their hindguts to use wood as a source of food. The lower termite R. flavipes houses a variety of protist and prokaryotes that are the key players the disassembly of lignocellulose. In this paper we describe the genomes and the gene expression profiles of five Endomicrobium endosymbionts living inside three different protist species from R. flavipes. Data from these genomes suggest that these Endomicrobium species have different mechanisms for using both carbon and nitrogen. In addition, they harbor genes that may be used to import free DNA from their environment. This process of DNA-uptake may cntribute to the high levels of horizontal gene transfer often seen in the Endomicrobium species.