‘Candidatus Adiutrix intracellularis’, an endosymbiont of termite gut flagellates, is the first representative of a deep‐branching clade of Deltaproteobacteria and a putative homoacetogen

Abstract

Termite gut flagellates are typically colonized by specific bacterial symbionts. Here we describe the phylogeny, ultrastructure and subcellular location of 'Candidatus Adiutrix intracellularis', an intracellular symbiont of Trichonympha collaris in the termite Zootermopsis nevadensis. It represents a novel, deep-branching clade of uncultured Deltaproteobacteria widely distributed in intestinal tracts of termites and cockroaches. Fluorescence in situ hybridization and transmission electron microscopy localized the endosymbiont near hydrogenosomes in the posterior part and near the ectosymbiont 'Candidatus Desulfovibrio trichonymphae' in the anterior part of the host cell. The draft genome of 'Ca. Adiutrix intracellularis' obtained from a metagenomic library revealed the presence of a complete gene set encoding the Wood-Ljungdahl pathway, including two homologs of fdhF encoding hydrogenase-linked formate dehydrogenases (FDHH ) and all other components of the recently described hydrogen-dependent carbon dioxide reductase (HDCR) complex, which substantiates previous claims that the symbiont is capable of reductive acetogenesis from CO2 and H2 . The close phylogenetic relationship between the HDCR components and their homologs in homoacetogenic Firmicutes and Spirochaetes suggests that the deltaproteobacterium acquired the capacity for homoacetogenesis via lateral gene transfer. The presence of genes for nitrogen fixation and the biosynthesis of amino acids and cofactors indicate the nutritional nature of the symbiosis.

Rampant Host Switching Shaped the Termite Gut Microbiome

“…animal guts, are likely to have been transferred through contact with soil or through feeding. The gut microbiota of lower termites contains many bacterial lineages that are specifically associated with the surface, the cytoplasm, or the nucleus of their symbiotic flagellates (e.g., [23][24][25]). Phylogenetic analyses have documented co-speciation between flagellates and their bacterial symbionts and flagellates [8,26,27], but co-cladogenesis between bacterial symbionts and termites remains an exception [8] because of the occasional horizontal transfer of flagellates between termites of different families.…”

The functional microbiome of arthropods

“…The listing of microbiome taxa was organized in rows that followed as close as possible the sequence derived from detailed phylogenetic analysis, from late diverging down to deep branching organisms in each class of proteobacteria. The phylogenetic position of the various taxa was evaluated by combining relevant studies on the phylogenesis of alpha [57–59], gamma [60–62] and delta proteobacteria [63–65] with detailed analysis of conserved proteins carried out as described earlier [37,38,49,62,66]. The proteins include the catalytic subunit of aa3- and bd-type oxidases, which are not present in all proteobacteria [37,62], the NuoD and NuoL subunits of complex I [38,49], the catalytic subunit of [FeFe]-hydrogenase [6,57], cytochrome b of the bc1 complex [66], the flavoprotein subunit SdhA of succinate dehydrogenase and its related protein of fumarate reductase [67].…”

Genome analysis of ‘Candidatus Ancillula trichonymphae’, first representative of a deep‐branching clade of Bifidobacteriales, strengthens evidence for convergent evolution in flagellate endosymbionts

“…1.1 Mbp; Hongoh et al, 2008b), 'Candidatus Treponema intracellularis' (2.7-3.2 Mbp; Ohkuma et al, 2015), 'Candidatus Adiutrix intracellularis ' (ca. 2.3 Mb;Ikeda-Ohtsubo et al, 2016) and 'Ca. A. trichonymphae' (ca.…”

“…By contrast, ammonia assimilation and nitrogen fixation are features that are not present in all flagellate endosymbionts. The capacity for ammonia assimilation, which was so far restricted to those endosymbionts that have the capacity for nitrogen fixation (Hongoh et al, 2008b;Ohkuma et al, 2015;Ikeda-Ohtsubo et al, 2016), is present in 'Ca. A. trichonymphae' (this study) but absent in 'Ca.…”

“…Noda et al, 2005;Stingl et al, 2005;Strassert et al, 2010;Sato et al, 2014;Ohkuma et al, 2015), the reconstructed genomes of the four endosymbionts investigated to date revealed a striking similarity in their metabolic capacities. Despite an often substantial genome reduction, the endosymbionts have retained the pathways involved in nitrogen metabolism, particularly the biosynthesis of amino acids, nucleic acids and cofactors and in some instances including the capacity for dinitrogen fixation and the assimilation of ammonia (Hongoh et al, 2008a,b;Ohkuma et al, 2015;Ikeda-Ohtsubo et al, 2016). Although little is known about the nutritional requirements of termite gut flagellates, it is assumed that the endosymbionts provide nutrients that would otherwise have to be acquired from the environment, e.g.…”