A meta-analysis testing eusocial co-option theories in termite gut physiology and symbiosis

Abstract

The termite gut accomplishes key physiologic functions that underlie termite symbiosis and sociality. However, potential candidate functions of the host-symbiont holobiome have not yet been explored across seemingly divergent processes such as digestion, immunity, caste differentiation, and xenobiotic tolerance. This study took a meta-analysis approach for concurrently studying host and symbiont gut metatranscriptome responses of the lower termite Reticulitermes flavipes, which has ancestral characteristics and hosts a diverse mix of eukaryotic and bacterial symbionts. Thirteen treatments were compared from 5 categories (dietary, social, hormonal, immunological, and xenobiotic), revealing 3 main insights. First, each of the 5 tested colonies had distinct magnitudes of transcriptome response, likely as a result of unique symbiont profiles, which highlights the uniqueness of individual termite colonies. Second, after normalization to standardize colony response magnitudes, unique treatment-linked metatranscriptome topologies became apparent. Third, despite colony and topology differences, 4 co-opted master genes emerged that were universally responsive across diverse treatments. These master genes encode host functions related to protein translation and symbiont functions related to protein degradation and pore formation in microbial cell walls. Three of the 4 master genes were from co-evolved protist symbionts, highlighting potentially co-evolved roles for gut symbiota in coordinating functional responses of the collective host-symbiont holobiome. Lastly, for host genes identified, these results provide annotations of recent termite genome sequences. By revealing conserved domain genes, as well as apparent roles for gut symbiota in holobiome regulation, this study provides new insights into co-opted eusocial genes and symbiont roles in termite sociobiology.

Soldier‐biased gene expression in a subterranean termite implies functional specialization of the defensive caste

“…This transcriptome is assembled from whole body tissue mRNAs sampled from three different North American populations. As such, it provides a reasonable estimate of gene composition and expression for this species that compliments prior genomic studies of Reticulitermes (Dedeine et al, 2015;Hayashi et al, 2013;Mitaka et al, 2016;Raychoudhury et al, 2013;Scharf et al, 2003;Scharf et al, 2005;Scharf et al, 2017;Sen et al, 2013;Steller et al, 2010; and other termites (Huang, Sun, Zhou, & Lei, 2012;Ishikawa et al, 2010;Korb et al, 2015;Koshikawa et al, 2005;Poulsen et al, 2014;Terrapon et al, 2014;Wu et al, 2016). Established indicators of transcriptome quality such as N50 value and average gene length generated for the present assembly (Table 3) are consistent with benchmark expectations for non-model organisms (Francis et al, 2013).…”

Transcriptome Responses to Defined Insecticide Selection Pressures in the German Cockroach (Blattella germanica L.)

“…In the present study, transcript contigs from representatives of all of these groups were greatly reduced with indoxacarb selection. Omics approaches similar to those used here have previously identified gregarines and other eukaryotic microbes in insects and thus it should not be surprising that similar eukaryotic microbe transcripts were identified in the present study through the use of poly-A RNA tagging (McCarthy et al, 2011;Scharf, 2015;Scharf et al, 2017). Many of the microbial genera that were reduced by the selection process are potential pathogens to humans and companion animals (e.g., Cryptosporidium, Toxoplasma, Vitrella, Plasmodium, Neospora, etc.)…”

Symbiotic flagellate protists as cryptic drivers of adaptation and invasiveness of the subterranean termite Reticulitermes grassei Clément

“…The remaining morphotypes may constitute facultative symbionts, which, although not being essential for host survival, may provide important benefits, acting like a horizontal gene pool that potentially influences host invasiveness and ecology (Henry et al., ; Kikuchi et al., ). The uniqueness of termite colony symbiotic communities has recently been shown for R. flavipes (Scharf et al., ).…”