Formyltetrahydrofolate Synthetase Gene Diversity in the Guts of Higher Termites with Different Diets and Lifestyles

Abstract

In this study, we examine gene diversity for formyl-tetrahydrofolate synthetase (FTHFS), a key enzyme in homoacetogenesis, recovered from the gut microbiota of six species of higher termites. The "higher" termites (family Termitidae), which represent the majority of extant termite species and genera, engage in a broader diversity of feeding and nesting styles than the "lower" termites. Previous studies of termite gut homoacetogenesis have focused on wood-feeding lower termites, from which the preponderance of FTHFS sequences recovered were related to those from acetogenic treponemes. While sequences belonging to this group were present in the guts of all six higher termites examined, treponeme-like FTHFS sequences represented the majority of recovered sequences in only two species (a wood-feeding Nasutitermes sp. and a palm-feeding Microcerotermes sp.). The remaining four termite species analyzed (a Gnathamitermes sp. and two Amitermes spp. that were recovered from subterranean nests with indeterminate feeding strategies and a litter-feeding Rhynchotermes sp.) yielded novel FTHFS clades not observed in lower termites. These termites yielded two distinct clusters of probable purinolytic Firmicutes and a large group of potential homoacetogens related to sequences previously recovered from the guts of omnivorous cockroaches. These findings suggest that the gut environments of different higher termite species may select for different groups of homoacetogens, with some species hosting treponeme-dominated homoacetogen populations similar to those of wood-feeding, lower termites while others host Firmicutes-dominated communities more similar to those of omnivorous cockroaches.The insect order Isoptera is divided into seven major families. Six of these families are comprised of "lower termites," which are exclusively wood and/or grass feeders. The "higher termites" are a single family (Termitidae), which nonetheless contains about 85% of known genera (10). Higher termites are able to utilize a much broader range of substrates than lower termites; in addition to wood and grass feeding, higher termite species have evolved fungus-cultivating, litter-and soil-feeding lifestyles. Higher termites with different feeding habits have been found to have vastly different complements of symbiotic bacteria (21,32,33,35).The symbiosis between termites and their gut microbes is a complex, obligate mutualism. The hindgut community acts as a highly efficient bioreactor, converting complex substrates to acetate, which constitutes the principal source of energy for the termite (22). In wood-feeding termites, H 2 is the central free intermediate in the degradation of lignocellulose, representing 18 to 26% of the termite's respiratory activity (27). The majority (83 to 100%) of this hydrogen is converted to acetate through homoacetogenesis (27). In contrast, soil-feeding and fungus-cultivating termites have been shown to have relatively lower rates of gut homoacetogenesis and higher rates of methanogenesis from H 2 and CO 2 (3), suggesting ...

The Cockroach Origin of the Termite Gut Microbiota: Patterns in Bacterial Community Structure Reflect Major Evolutionary Events

“…The latter was most obvious in the spirochetal cluster Treponema Ia and matches the dominance of Spirochaetes in the guts of wood-feeding termites (11,42). Since this cluster comprises the homoacetogenic Treponema primitia (46), its upshift is also consistent with changes in the distributions of several functional marker genes (formyltetrahydrofolate synthetase, CO dehydrogenase, and hydrogenase) (47)(48)(49), which indicated that the bacteria responsible for reductive acetogenesis in omnivorous cockroaches are not the same as those in wood-feeding termites and C. punctulatus. Several of the genus level taxa that predominated only in lower termites (Fig.…”

Patterns of [FeFe] Hydrogenase Diversity in the Gut Microbial Communities of Lignocellulose-Feeding Higher Termites

“…JT5 and Amitermes sp. JT2 were found to be the most closely related of any of the higher termites used in this study (38). Correspondingly, there was a tendency for sequences from Gnathamitermes sp.…”

“…Analyses of spirochete diversity in higher and lower termites have demonstrated a tendency of spirochete 16S sequences from the same genus of termite to cluster with one another, supporting the hypothesis that "spirochaetes are specific symbionts that have coevolved with their respective species of termites" (4,36). Moreover, the composition of termite gut communities has been shown to vary substantially with host feeding habits, which are closely linked with phylogeny (32,38,44). In the case of wood roaches, a very close correspondence of host and symbiont phylogenies has lent strong support for the cospeciation of a Cryptocercus endosymbiont with its hosts (16,19,28).…”

“…folate synthetase gene diversity reported by Ottesen and Leadbetter on the very same two gut samples analyzed in this study (38). The Rhyncotermes termites were gathered from a colony that appeared to be feeding on a compost pile containing a mixture of woody and leaf detritus, which may have the consequence of a broader diversity of bacteria within its gut environment.…”

“…JOTR:2008-SCI-002). Termites were identified in a previous study (38) using insect mitochondrial cytochrome oxidase subunit II (COXII) gene sequences and morphology.…”