Open Access

Background Spirochetes are the most abundant bacterial group in the hindgut of termites. The largest species, with cell lengths of up to 100 µm, have been provisionally classified in the family “Pillotinaceae” based exclusively on morphological traits. However, in the absence of cultured representatives, their phylogenetic position and metabolism remain entirely unknown. Results We investigated phylogeny and metabolic capacities of “pillotinaceous” spirochetes using single-cell techniques, electron microscopy, and fluorescence in situ hybridization. All sequences of large spirochetes obtained from various termites fell into four distinct, well-supported clusters within the family Breznakiellaceae. Based on ultrastructural features, three of the clusters were assigned to the genera Pillotina, Hollandina, and the newly established genus Hollandinoides; a fourth cluster was tentatively assigned to the genus Clevelandina. Functional analysis of the single-cell genomes of Pillotina corrugata sp. nov., Hollandina grandis sp. nov., and Hollandinoides gharagozlouae gen. nov. sp. nov., combined with comparative genomics of other uncultured relatives, demonstrated differences in the capacity to degrade cellulose, hemicelluloses, and dextrins. While members of the genus Pillotina have a fermentative metabolism, members of the other genera encode a Wood–Ljungdahl pathway and, in the case of Hollandina, a group-III nitrogenase, suggesting roles in reductive acetogenesis and nitrogen fixation. Conclusions Our results provide the first molecular data on pillotinaceous spirochetes. We show that the three genera covered in our study belong to the family Breznakiellaceae, which harbors the majority of termite-gut spirochetes. Comparative genome analysis indicated that the large spirochetes in termite guts have distinct roles in symbiotic digestion.

Horizontal gene transfer (HGT), the transmission of genetic material across species, is an important innovation source in prokaryotes. In contrast, its significance is unclear in many eukaryotes, including insects. Here, we used high-quality genomes of 45 termites and two cockroaches to investigate HGTs from non-metazoan organisms across blattodean genomes. We identified 289 genes and 2,494 pseudogenes classified into 168 orthologous groups originating from an estimated 281 HGT events. Wolbachia represented the primary HGT source, while termite gut bacteria and the cockroach endosymbiont Blattabacterium did not contribute meaningfully to HGTs. Most horizontally acquired genes descended from recent and species-specific HGTs, experienced frequent duplications and pseudogenizations, and accumulated substitutions faster than synonymous sites of native protein-coding genes. Genes frequently transferred horizontally to termite genomes included mobile genetic elements and genetic information processing genes. Our results indicate that termites continuously acquired genes through HGT, and that most horizontally acquired genes are specific to restricted lineages. Overall, genes acquired by HGT by termites and cockroaches seemed generally non-functional and bound to be lost.

Termites are a lineage of social cockroaches abundant in tropical ecosystems where they are key decomposers of organic matter. Despite their ecological significance, only a handful of reference-quality termite genomes have been sequenced, which is insufficient to unravel the genetic mechanisms that have contributed to their ecological success. Here, we perform sequencing and hybrid assembly of 45 taxonomically and ecologically diverse termites and two cockroaches, resulting in haplotype-merged genome assemblies of 47 species, 22 of which were near-chromosome level. Next, we examine the link between termite dietary evolution and major genomic events. We find that Termitidae, which include ~80% of described termite species, have larger genomes with more genes and a higher proportion of transposons than other termites. Our analyses identify a gene number expansion early in the evolution of Termitidae, including an expansion of the repertoire of CAZymes, the genes involved in lignocellulose degradation. Notably, this expansion of genomes and gene repertoires coincided with the origin of soil-feeding in Termitidae and remained unchanged in lineages that secondarily reverted to a wood-based diet. Overall, our sequencing effort multiplies the number of available termite genomes by six and provides insights into the genome evolution of an ancient lineage of social insects.

Termites challenge long-standing assumptions about insect social evolution. One important difference compared to the social ants, bees and wasps lies in their chromosomes: termites are diploid, with X/Y sex differentiation observed in most species and males playing active roles across all castes and life stages. Adding to their uniqueness, termites exhibit multivalent chromosome chains during male meiosis—an intriguing and seldom seen feature of eukaryote evolution. These chains, in addition to other chromosomal formations, such as bivalent rings and rods, may serve to suppress recombination, thereby mitigating against the potentially harmful effects of inbreeding. Again, this positions termites as an important contrasting study system to other social insect groups, where recombination rates tend to be elevated. Multivalent chromosome chains may also play a significant role in speciation processes by increasing the likelihood of chromosomal translocations and promoting genomic islands of divergence. In European Reticulitermes, variability in chain length and stability both between and within species provides a compelling model system for studying the evolutionary importance of multivalent chromosome chains at intra- and interspecific levels and at different evolutionary time scales. To investigate these dynamics, we collected over 200 colonies of Reticulitermes species across the Mediterranean, generating de novo reference genomes, comprehensive population genomic as well as karyotypic data from three recently diverged species. Our findings shed light on the intricate relationship between chromosomal architecture and evolutionary mechanisms in termites, offering new insight into how genome structure shapes species evolution.

Immunity plays an important role in evolutionary ecology. The immune system interacts with both pathogens, which can act as important selective forces, and symbionts, which are regulated by the host‘s immune system and can also play a role in the host‘s immune defenses. The Blattodea consist of what is commonly known as cockroaches and the termites, who are themselves specialized eusocial cockroaches. Blattodea have two symbiont types that are characteristic to either the cockroaches or the termites (Table 1). These symbiont transitions open up the opportunity to characterize and investigate host-symbiont-pathogen interactions and how they evolved in Blattodea.