The Role of Host Phylogeny Varies in Shaping Microbial Diversity in the Hindguts of Lower Termites

Abstract

eThe hindguts of lower termites and Cryptocercus cockroaches are home to a distinct community of archaea, bacteria, and protists (primarily parabasalids and some oxymonads). Within a host species, the composition of these hindgut communities appears relatively stable, but the evolutionary and ecological factors structuring community composition and stability are poorly understood, as are differential impacts of these factors on protists, bacteria, and archaea. We analyzed the microbial composition of parabasalids and bacteria in the hindguts of Cryptocercus punctulatus and 23 species spanning 4 families of lower termites by pyrosequencing variable regions of the small-subunit rRNA gene. Especially for the parabasalids, these data revealed undiscovered taxa and provided a phylogenetic basis for a more accurate understanding of diversity, diversification, and community composition. The composition of the parabasalid communities was found to be strongly structured by the phylogeny of their hosts, indicating the importance of historical effects, although exceptions were also identified. Particularly, spirotrichonymphids and trichonymphids likely were transferred between host lineages. In contrast, host phylogeny was not sufficient to explain the majority of bacterial community composition, but the compositions of the Bacteroidetes, Elusimicrobia, Tenericutes, Spirochaetes, and Synergistes were structured by host phylogeny perhaps due to their symbiotic associations with protists. All together, historical effects probably resulting from vertical inheritance have had a prominent role in structuring the hindgut communities, especially of the parabasalids, but dispersal and environmental acquisition have played a larger role in community composition than previously expected.C ryptocercus cockroaches and their sister lineage, the lower termites (1), are both dependent on diverse communities of microorganisms in their hindguts to gain nutrition from lignocellulose (reviewed in references 2 and 3). These are fascinating and complex communities dominated by parabasalid (Parabasalia) and oxymonad (Preaxostyla) protists (4) as well as numerous bacterial lineages, including Actinobacteria, Bacteroidetes, Elusimicrobia, Firmicutes, Proteobacteria, Spirochaetes,. Moreover, a large proportion of the bacteria form obligate symbiotic interactions with the protists (see, for example, references 8-14), so the community contains multiple levels of symbiosis. Because of the diversity of symbionts, the hindguts of Cryptocercus cockroaches and lower termites can be used as model systems to study the ecology and interactions between protists and bacteria. Here, we investigate the ecological and evolutionary differences between protists and bacteria in structuring community composition. These differences are critical to understanding the diversification and adaptation of microbes, the stability and resilience of community structure, and the maintenance of ecosystem functions, particularly in regard to understanding lignocellulose digestion...

Molecular investigation of Australian termites and their gut symbionts

“…The 16 termite genera examined in this study have a set of core and accessory gut bacterial phyla that distinguish them from all other habitats ( Table 2.2). This observation is consistent with previous culture-independent studies which show that the combination of these phyla is highly distinctive of the termite gut microbiome (Warnecke et al, 2007;Hongoh, 2010;Tai et al, 2015) particularly in comparison to other insect gut communities (Douglas, 2009;Engel and Moran, 2013). This distinctiveness is further underlined by the observation that the majority of operational taxonomic units (OTUs) identified in the present study cluster with sequences from previous termite surveys ( Tholen and Brune, 1999;Hongoh et al, 2003;Shinzato et al, 2005;Yang et al, 2005;Nakajima et al, 2006;Warnecke and Hugenholtz, 2007;Köhler et al, 2008;Husseneder, 2010;Ikeda-Ohtsubo et al, 2010;Schauer et al, 2012).…”

“…Most members of Elusimicrobia and Euryarchaeota are intracellular bacterial symbionts of flagellates in the gut of lower termites and wood-feeding cockroaches (Cryptocercus punctulatus) (Ohkuma, 2008;Strassert et al, 2012), although a small number of Euryarchaeota such as some Methanobrevibacter are attached to the gut epithelial wall. Although only a relatively small percentage of Mastotermes protists were detected in this study as an artefact of the universal primers that do not target many microbial eukaryotes (see Chapter 2), it has been well demonstrated that flagellates make up the bulk of the microbial community in lower termites (Brune and Stingl, 2006;Tai et al, 2015). A declining trend in relative abundance of detected protists was observed between day four to day seven in all feeding treatments (Figure 3.5 Microbial gut community composition was analysed in greater detail using 97% identity operational taxonomic units (OTU) (Figure 3.6 and Appendix C: Table S3.1).…”

“…As noted in Chapter 2, diet appears to be a secondary signal in shaping the termite gut microbiota of both lower and higher termites when considering both protist and prokaryotic communities. Diet however appears as a driving factor influencing the gut community structure when only bacterial communities, likely acquired from the environment, are taken into consideration (Leber and Balkwill, 1997;Tai et al, 2015). It is not surprising that such conclusions are drawn as most of the SSU rRNA surveys have extensively been applied to the identification of prokaryotic populations in the termite gut.…”

The holobiont concept: the case of xylophagous termites and cockroaches

“…As noted above, symbiotic flagellates were established in an ancestor common to Cryptocercus and lower termites, vertically transmitted to their offspring through proctodeal interaction and subsequently became highly diversified depending on the host and the symbiont lineages Tai et al 2014). While lower termites and Cryptocercus support a characteristic community of gut protists, many protist species are not necessarily restricted to one termite species.…”

“…All endogenous (provided by the termite) GH are affiliated with the glycoside hydrolase family (GHF) 9, and GHF1 (Ni and Tokuda 2013). The hindgut microbiota of insects is largely structured by exogenous (diet and local environment) and endogenous (gut environment) factors (Colman et al 2012;Tai et al 2014;Yun et al 2014), but a dynamic core gut microbiota (commensal/symbiotic) were maintained even after environmental shifts ( Schauer et al 2014;Makonde et al 2015). Figure 4 shows the gut microbial composition at phylum level of several wood-feeding insect, including two omnivores' cockroaches.…”