Cultivable, Host-Specific <i>Bacteroidetes</i> Symbionts Exhibit Diverse Polysaccharolytic Strategies

Abstract

Beneficial gut microbes can facilitate insect growth on diverse diets. The omnivorous American cockroach, <i>Periplaneta americana</i> (Insecta: Blattodea), thrives on a diet rich in plant polysaccharides and harbors a species-rich gut microbiota responsive to host diet. <i>Bacteroidetes</i> are among the most abundant taxa in <i>P. americana</i> and other cockroaches, based on cultivation-independent gut community profiling, and these potentially polysaccharolytic bacteria may contribute to host diet processing. Eleven <i>Bacteroidetes</i> isolates were cultivated from <i>P. americana</i> digestive tracts, and phylogenomic analyses suggest that they were new <i>Bacteroides</i>, <i>Dysgonomonas</i>, <i>Paludibacter</i>, and <i>Parabacteroides</i> species distinct from those previously isolated from other insects, humans, and environmental sources. In addition, complete genomes were generated for each isolate, and polysaccharide utilization loci (PULs) and several non-PUL-associated carbohydrate-active enzyme (CAZyme)-coding genes that putatively target starch, pectin, and/or cellulose were annotated in each of the isolate genomes. Type IX secretion system (T9SS)- and CAZyme-coding genes tagged with the corresponding T9SS recognition and export C-terminal domain were observed in some isolates, suggesting that these CAZymes were deployed via non-PUL outer membrane translocons. Additionally, single-substrate growth and enzymatic assays confirmed genomic predictions that a subset of the <i>Bacteroides</i> and <i>Dysgonomonas</i> isolates could degrade starch, pectin, and/or cellulose and grow in the presence of these substrates as a single sugar source. Plant polysaccharides enrich <i>P. americana</i> diets, and many of these gut isolates are well equipped to exploit host dietary inputs and potentially contribute to gut community and host nutrient accessibility.<b>IMPORTANCE</b> Gut microbes are increasingly being recognized as critical contributors to nutrient accessibility in animals. The globally distributed omnivorous American cockroach (<i>Periplaneta americana</i>) harbors many bacterial phyla (e.g., <i>Bacteroidetes</i>) that are abundant in vertebrates. <i>P. americana</i> thrives on a highly diverse plant-enriched diet, making this insect a rich potential source of uncharacterized polysaccharolytic bacteria. We have cultivated, completely sequenced, and functionally characterized several novel <i>Bacteroidetes</i> species that are endemic to the <i>P. americana</i> gut, and many of these isolates can degrade simple and complex polysaccharides. Cultivation and genomic characterization of these <i>Bacteroidetes</i> isolates further enable deeper insight into how these taxa participate in polysaccharide metabolism and, more broadly, how they affect animal health and development.