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Division of functional roles for termite gut protists revealed by single-cell transcriptomes.

ABSTRACT: The microbiome in the hindgut of wood-feeding termites comprises various species of bacteria, archaea, and protists. This gut community is indispensable for the termite, which thrives solely on recalcitrant and nitrogen-poor wood. However, the difficulty in culturing these microorganisms has hindered our understanding of the function of each species in the gut. Although protists predominate in the termite gut microbiome and play a major role in wood digestion, very few culture-independent studies have explored the contribution of each species to digestion. Here, we report single-cell transcriptomes of four protists species comprising the protist population in worldwide pest Coptotermes formosanus. Comparative transcriptomic analysis revealed that the expression patterns of the genes involved in wood digestion were different among species, reinforcing their division of roles in wood degradation. Transcriptomes, together with enzyme assays, also suggested that one of the protists, Cononympha leidyi, actively degrades chitin and assimilates it into amino acids. We propose that C. leidyi contributes to nitrogen recycling and inhibiting infection from entomopathogenic fungi through chitin degradation. Two of the genes for chitin degradation were further revealed to be acquired via lateral gene transfer (LGT) implying the importance of LGT in the evolution of symbiosis. Our single-cell-based approach successfully characterized the function of each protist in termite hindgut and explained why the gut community includes multiple species.

SUBMITTER: Nishimura Y

PROVIDER: S-EPMC7490689 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BackgroundCiliated protists are a widely distributed, morphologically diverse, and genetically heterogeneous group of unicellular organisms, usually known for containing two types of nuclei: a transcribed polyploid macronucleus involved in gene expression and a silent diploid micronucleus responsible for transmission of genetic material during sexual reproduction and generation of the macronucleus. Although studies in a few species of culturable ciliated protists have revealed the highly dynamic nature of replicative and recombination events relating the micronucleus to the macronucleus, the broader understanding of the genomic diversity of ciliated protists, as well as their phylogenetic relationships and metabolic potential, has been hampered by the inability to culture numerous other species under laboratory conditions, as well as the presence of symbiotic bacteria and microalgae which provide a challenge for current sequencing technologies. Here, we optimized single-cell sequencing methods and associated data analyses, to effectively remove contamination by commensal bacteria, and generated high-quality genomes for a number of Euplotia species.ResultsWe obtained eight high-quality Euplotia genomes by using single-cell genome sequencing techniques. The genomes have high genomic completeness, with sizes between 68 and 125 M and gene numbers between 14K and 25K. Through comparative genomic analysis, we found that there are a large number of gene expansion events in Euplotia genomes, and these expansions are closely related to the phenotypic evolution and specific environmental adaptations of individual species. We further found four distinct subgroups in the genus Euplotes, which exhibited considerable genetic distance and relative lack of conserved genomic syntenies. Comparative genomic analyses of Uronychia and its relatives revealed significant gene expansion associated with the ciliary movement machinery, which may be related to the unique and strong swimming ability.ConclusionsWe employed single-cell genomics to obtain eight ciliate genomes, characterized the underestimated genomic diversity of Euplotia, and determined the divergence time of representative species in this subclass for the first time. We also further investigated the extensive duplication events associated with speciation and environmental adaptation. This study provides a unique and valuable resource for understanding the evolutionary history and genetic diversity of ciliates.

Project description:Some of the 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, as follows: Pyrsonympha vertens, Trichonympha agilis, and Dinenympha species II. Since these protist hosts represented members of different taxa which colonize separate 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 some possible niche-specific traits, such as carbon metabolism. Our analyses suggest that species-specific genes related to carbon metabolism were acquired by horizontal gene transfer (HGT) and may have come from taxa which are common in the termite hind gut. In addition, our analyses suggested that these endosymbionts contain and express genes related to natural transformation (competence) and recombination. Taken together, the presence of genes acquired by HGT and a putative competence pathway suggest that these endosymbionts are not cut off from gene flow and that competence may be a mechanism by which members of Endomicrobium can acquire new traits. IMPORTANCE The composition and structure of wood, which contains cellulose, hemicellulose, and lignin, prevent most organisms from using this common food source. Termites are a rare exception among animals, and they rely on a complex microbiota housed in their hindguts to use wood as a source of food. The lower termite, Reticulitermes flavipes, houses a variety of protists and prokaryotes that are the key players in the disassembly of lignocellulose. Here, 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 carbon. In addition, they harbor genes that may be used to import DNA from their environment. This process of DNA uptake may contribute to the high levels of horizontal gene transfer noted previously in Endomicrobium species.

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Division of functional roles for termite gut protists revealed by single-cell transcriptomes.

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