Parallel and Gradual Genome Erosion in the Blattabacterium Endosymbionts of Mastotermes darwiniensis and Cryptocercus Wood Roaches

Abstract

Almost all examined cockroaches harbor an obligate intracellular endosymbiont, Blattabacterium cuenoti. On the basis of genome content, Blattabacterium has been inferred to recycle nitrogen wastes and provide amino acids and cofactors for its hosts. Most Blattabacterium strains sequenced to date harbor a genome of ∼630 kbp, with the exception of the termite Mastotermes darwiniensis (∼590 kbp) and Cryptocercus punctulatus (∼614 kbp), a representative of the sister group of termites. Such genome reduction may have led to the ultimate loss of Blattabacterium in all termites other than Mastotermes. In this study, we sequenced 11 new Blattabacterium genomes from three species of Cryptocercus in order to shed light on the genomic evolution of Blattabacterium in termites and Cryptocercus. All genomes of Cryptocercus-derived Blattabacterium genomes were reduced (∼614 kbp), except for that associated with Cryptocercus kyebangensis, which comprised 637 kbp. Phylogenetic analysis of these genomes and their content indicates that Blattabacterium experienced parallel genome reduction in Mastotermes and Cryptocercus, possibly due to similar selective forces. We found evidence of ongoing genome reduction in Blattabacterium from three lineages of the C. punctulatus species complex, which independently lost one cysteine biosynthetic gene. We also sequenced the genome of the Blattabacterium associated with Salganea taiwanensis, a subsocial xylophagous cockroach that does not vertically transmit gut symbionts via proctodeal trophallaxis. This genome was 632 kbp, typical of that of nonsubsocial cockroaches. Overall, our results show that genome reduction occurred on multiple occasions in Blattabacterium, and is still ongoing, possibly because of new associations with gut symbionts in some lineages.

Inhibition of a nutritional endosymbiont by glyphosate abolishes mutualistic benefit on cuticle synthesis in Oryzaephilus surinamensis

“…Whether the O. surinamensis symbiont can recycle nitrogen, like Blattabacterium sp. 57 , 58 remains unclear, as it encodes the urease α and γ subunits ( ureC [EC:3.5.1.5]), but no glutamate dehydrogenase ( gdhA ) that would allow integrating the resulting ammonium into the amino acid metabolism via glutamate was detected. Instead, it encodes a proline transporter ( opuE ), proline dehydrogenase [EC:1.5.5.2], and oxidoreductase [EC:1.2.1.88] to import and convert proline into glutamate 59 , 60 , which may then be exported to function as an amino group donor for the synthesis of the aromatic amino acids from chorismate/prephenate by the beetle itself 19 .…”

Enhanced Mutation Rate, Relaxed Selection, and the “Domino Effect” are associated with Gene Loss in Blattabacterium, A Cockroach Endosymbiont

“…Several lineages independently experienced further reduction and have genomes as small as 511 kb ( López-Sánchez et al 2009 ; Sabree et al 2009 ; Neef et al 2011 ; Huang et al 2012 ; Sabree et al 2012 ; Kambhampati et al 2013 ; Patiño-Navarrete et al 2013 ; Tokuda et al 2013 ; Kinjo et al 2015 , 2018 ; Vicente et al 2018 ; Bourguignon et al 2020 ). For example, the sister strains of Blattabacterium associated with the woodroach Cryptocercus punctulatus and M. darwiniensis have reduced genomes of 610 and 590 kb, respectively, and have experienced independent genome reduction, as indicated by the relatively large 637 kb genome of the strain of Cryptocercus kyebangensis ( Kinjo et al 2018 ). Interestingly, many genes involved in amino acid biosynthesis were lost in parallel in both strains ( Kinjo et al 2018 ), possibly compensated by the stable association their host established with their largely vertically transmitted gut microbes ( Brune 2014 ).…”

“…For example, the sister strains of Blattabacterium associated with the woodroach Cryptocercus punctulatus and M. darwiniensis have reduced genomes of 610 and 590 kb, respectively, and have experienced independent genome reduction, as indicated by the relatively large 637 kb genome of the strain of Cryptocercus kyebangensis ( Kinjo et al 2018 ). Interestingly, many genes involved in amino acid biosynthesis were lost in parallel in both strains ( Kinjo et al 2018 ), possibly compensated by the stable association their host established with their largely vertically transmitted gut microbes ( Brune 2014 ). How common parallel gene loss is in Blattabacterium remains to be understood.…”

Evolutionary rates are correlated between cockroach symbionts and mitochondrial genomes

“…The genomes of 21 Blattabacterium strains sequenced to date are highly reduced compared with those of their free-living relatives, ranging in size from 590 to 645 kb [16][17][18][19][20]. They contain genes encoding enzymes for DNA replication and repair, with some exceptions (holA, holB and mutH) [16][17][18][19][20]. The extent to which host nuclear proteins are involved in the cell biology of Blattabacterium, and particularly DNA replication, is not well understood.…”