Evidence for reduced immune gene diversity and activity during the evolution of termites

This study was supported by Freie Universität Internal Research Funding and Devtsche Forschungsgemeinschaft (DFG, grant no. MC 436/5-1) to D.P.M. S.H., P.S. and J.S. are supported by ‘EVA4.0’ (no. CZ.02.1.01/0.0/0.0/16_019/0000803), and P.S. and J.S. are supported by CIGA no. 20184306. Y.C. and Z.W. are supported by the National Natural Science Foundation of China (grant no. 31672329).The evolution of biological complexity is associated with the emergence of bespoke immune systems that maintain and protect organism integrity. Unlike the well-studied immune systems of cells and individuals, little is known about the origins of immunity during the transition to eusociality, a major evolutionary transition comparable to the evolution of multicellular organisms from single-celled ancestors. We aimed to tackle this by characterizing the immune gene repertoire of 18 cockroach and termite species, spanning the spectrum of solitary, subsocial and eusocial lifestyles. We find that key transitions in termite sociality are correlated with immune gene family contractions. In cross-species comparisons of immune gene expression, we find evidence for a caste-specific social defence system in termites, which appears to operate at the expense of individual immune protection. Our study indicates that a major transition in organismal complexity may have entailed a fundamental reshaping of the immune system optimized for group over individual defence.Peer reviewe

The oral gland, a new exocrine organ of termites

Termites have a rich set of exocrine glands. These glands are located all over the body, appearing in the head, thorax, legs and abdomen. Here, we describe the oral gland, a new gland formed by no more than a few tens of Class I secretory cells. The gland is divided into two secretory regions located just behind the mouth, on the dorsal and ventral side of the pharynx, respectively. The dominant secretory organelle is a smooth endoplasmic reticulum. Secretion release is under direct control of axons located within basal invaginations of the secretory cells. The secretion is released through a modified porous cuticle located at the mouth opening. We confirmed the presence of the oral gland in workers and soldiers of several wood- and soil-feeding species of Rhinotermitidae and Termitidae, suggesting a broader distribution of the oral gland among termites. The oral gland is the smallest exocrine gland described in termites so far. We hypothesise that the oily secretion can either ease the passage of food or serve as a primer pheromone

Termites host specific fungal communities that differ from those in their ambient environments

Termites are important plant biomass decomposers. Their digestive activity typically relies on prokaryotes and protozoa present in their guts. In some cases, such as in fungus-growing termites, digestion also relies on ectosymbiosis with specific fungal taxa. To date, the mycobiome of termites has yet to be investigated in detail. We evaluated the specificity of whole-termite associated fungal communities in three wood-feeding termite species. We showed that the whole-termite fungal community spectra are stable over diverse environments, regardless of the host species, and differ markedly from the wood in which they nest. The core mycobiome is similar to that found in other ecologically related insects and consists of a narrow spectrum of common filamentous fungi and yeasts, known for their stress tolerance and their ability to decompose plant biomass. The observed patterns suggest that a number of fungal strains may have a symbiotic relationship with termites, and our results set the stage for future investigations into the interactions between fungi, termites, and their other gut microbiota

Termites Are Associated with External Species-Specific Bacterial Communities

All termites have established a wide range of associations with symbiotic microbes in their guts. Some termite species are also associated with microbes that grow in their nests, but the prevalence of these associations remains largely unknown. Here, we studied the bacterial communities associated with the termites and galleries of three wood-feeding termite species by using 16S rRNA gene amplicon sequencing. We found that the compositions of bacterial communities among termite bodies, termite galleries, and control wood fragments devoid of termite activities differ in a species-specific manner. Termite galleries were enriched in bacterial operational taxonomic units (OTUs) belonging to Rhizobiales and Actinobacteria, which were often shared by several termite species. The abundance of several bacterial OTUs, such as Bacillus, Clostridium, Corynebacterium, and Staphylococcus, was reduced in termite galleries. Our results demonstrate that both termite guts and termite galleries harbor unique bacterial communities.IMPORTANCE As is the case for all ecosystem engineers, termites impact their habitat by their activities, potentially affecting bacterial communities. Here, we studied three wood-feeding termite species and found that they influence the composition of the bacterial communities in their surrounding environment. Termite activities have positive effects on Rhizobiales and Actinobacteria abundance and negative effects on the abundance of several ubiquitous genera, such as Bacillus, Clostridium, Corynebacterium, and Staphylococcus. Our results demonstrate that termite galleries harbor unique bacterial communities

Evidence for reduced immune gene diversity and activity during the evolution of termites

The evolution of biological complexity is associated with the emergence of bespoke immune systems that maintain and protect organism integrity. Unlike the well-studied immune systems of cells and individuals, little is known about the origins of immunity during the transition to eusociality, a major evolutionary transition comparable to the evolution of multicellular organisms from single-celled ancestors. We aimed to tackle this by characterizing the immune gene repertoire of 18 cockroach and termite species, spanning the spectrum of solitary, subsocial and eusocial lifestyles. We find that key transitions in termite sociality are correlated with immune gene family contractions. In cross-species comparisons of immune gene expression, we find evidence for a caste-specific social defence system in termites, which appears to operate at the expense of individual immune protection. Our study indicates that a major transition in organismal complexity may have entailed a fundamental reshaping of the immune system optimized for group over individual defence

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Complete mitochondrial genome of the drywood termite Cryptotermes havilandi (Isoptera: Kalotermitidae)

We report the first complete mitochondrial genome of an important pest of timber, the drywood termite Cryptotermes havilandi. The gene content and synteny of the mitochondrial genome of C. havilandi is identical to that of other termite species reported to date. It is composed 13 protein-coding genes, two ribosomal RNA genes, and 22 transfer RNA genes. Our phylogenetic tree, that includes the mitochondrial genomes of 14 species of Kalotermitidae, including C. havilandi, resolves the phylogenetic position of C. havilandi within Kalotermitidae

Phylogenomic analysis of 589 metagenome-assembled genomes encompassing all major prokaryotic lineages from the gut of higher termites

International audience“Higher” termites have been able to colonize all tropical and subtropical regions because of their ability to digest lignocellulose with the aid of their prokaryotic gut microbiota. Over the last decade, numerous studies based on 16S rRNA gene amplicon libraries have largely described both the taxonomy and structure of the prokaryotic communities associated with termite guts. Host diet and microenvironmental conditions have emerged as the main factors structuring the microbial assemblages in the different gut compartments. Additionally, these molecular inventories have revealed the existence of termite-specific clusters that indicate coevolutionary processes in numerous prokaryotic lineages. However, for lack of representative isolates, the functional role of most lineages remains unclear. We reconstructed 589 metagenome-assembled genomes (MAGs) from the different gut compartments of eight higher termite species that encompass 17 prokaryotic phyla. By iteratively building genome trees for each clade, we significantly improved the initial automated assignment, frequently up to the genus level. We recovered MAGs from most of the termite-specific clusters in the radiation of, for example, Planctomycetes, Fibrobacteres, Bacteroidetes, Euryarchaeota, Bathyarchaeota, Spirochaetes, Saccharibacteria, and Firmicutes, which to date contained only few or no representative genomes. Moreover, the MAGs included abundant members of the termite gut microbiota. This dataset represents the largest genomic resource for arthropod-associated microorganisms available to date and contributes substantially to populating the tree of life. More importantly, it provides a backbone for studying the metabolic potential of the termite gut microbiota, including the key members involved in carbon and nitrogen biogeochemical cycles, and important clues that may help cultivating representatives of these understudied clades