High-Resolution Analysis of Gut Environment and Bacterial Microbiota Reveals Functional Compartmentation of the Gut in Wood-Feeding Higher Termites (Nasutitermes spp.)

Abstract

<jats:title>ABSTRACT</jats:title><jats:p>Higher termites are characterized by a purely prokaryotic gut microbiota and an increased compartmentation of their intestinal tract. In soil-feeding species, each gut compartment has different physicochemical conditions and is colonized by a specific microbial community. Although considerable information has accumulated also for wood-feeding species of the genus<jats:named-content content-type="genus-species">Nasutitermes</jats:named-content>, including cellulase activities and metagenomic data, a comprehensive study linking physicochemical gut conditions with the structure of the microbial communities in the different gut compartments is lacking. In this study, we measured high-resolution profiles of H<jats:sub>2</jats:sub>, O<jats:sub>2</jats:sub>, pH, and redox potential in the gut of<jats:named-content content-type="genus-species">Nasutitermes corniger</jats:named-content>termites, determined the fermentation products accumulating in the individual gut compartments, and analyzed the bacterial communities in detail by pyrotag sequencing of the V3-V4 region of the 16S rRNA genes. The dilated hindgut paunch (P3 compartment) was the only anoxic gut region, showed the highest density of bacteria, and accumulated H<jats:sub>2</jats:sub>to high partial pressures (up to 12 kPa). Molecular hydrogen is apparently produced by a dense community of<jats:named-content content-type="genus-species">Spirochaetes</jats:named-content>and<jats:named-content content-type="genus-species">Fibrobacteres</jats:named-content>, which also dominate the gut of other<jats:named-content content-type="genus-species">Nasutitermes</jats:named-content>species. All other compartments, such as the alkaline P1 compartment (average pH, 10.0), showed high redox potentials and comprised small but distinct populations characteristic for each gut region. In the crop and the posterior hindgut compartments, the community was even more diverse than in the paunch. Similarities in the communities of the posterior hindgut and crop suggested that proctodeal trophallaxis or coprophagy also occurs in higher termites. The large sampling depths of pyrotag sequencing in combination with the determination of important physicochemical parameters allow cautious conclusions concerning the functions of particular bacterial lineages in the respective gut sections to be drawn.</jats:p>

The gut microbiota of the wood-feeding termite Reticulitermes lucifugus (Isoptera; Rhinotermitidae)

“…The gut can be described as an anaerobic gradient system which is constantly supplied with oxygen via the epithelium (Köhler et al 2012). The gut microbiota is commonly exchanged between colony members and transmitted to the next generation via trophallaxis (proctodeal feeding), which can promote coevolutional diversification of symbiotic microbes along with host phylogeny (Tokuda et al 2014).…”

The holobiont concept: the case of xylophagous termites and cockroaches

“…Oxygen penetrates the contents of the peripheral hindgut to a depth of 150-200 μm below the epithelium. The removal of oxygen by the respiratory activity of the gut microbiota creates a micro-oxic periphery around a highly anoxic center (Brune and Friedrich 2000;Köhler et al 2012). …”

Development of an ecophysiological model for Diplosphaera colotermitum TAV2, a termite hindgut Verrucomicrobium

“…Among the domain Bacteria, members of the phylum Verrucomicrobia have been consistently detected in molecular surveys of the 16S rRNA gene targeting the microbial community of various termite species (Hongoh et al, 2003;Nakajima et al, 2005;Berlanga et al, 2011;Rosengaus et al, 2011;Kö hler et al, 2012). Despite their ubiquity in higher and lower termite species, their functional role remains elusive.…”

“…It has been long assumed that prokaryotic residents, in the hypoxic periphery of the termite gut, have the primary role of consuming O 2 and maintaining a steep radial gradient of this inwardly diffusing gas resulting in anoxia in the luminal portion of the gut (Brune et al, 1995;Kö hler et al, 2012). However, this assumption has recently been challenged by the demonstration of a strong correlation between the O 2 consumption rate of extracted guts and the number of protozoans per gut (Wertz and Breznak, 2007b), suggesting a more modest role for bacteria in this process-at least in those termites that possess (putatively 'strictly' anaerobic) cellulolytic protozoa in their hindguts.…”