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

Abstract

Intracellular endosymbionts have reduced genomes that progressively lose genes at a timescale of tens of million years. We previously reported that gene loss rate is linked to mutation rate in Blattabacterium, however, the mechanisms causing gene loss are not yet fully understood. Here, we carried out comparative genomic analyses on the complete genome sequences of a representative set of 67 Blattabacterium strains, with sizes ranging between 511kbp and 645kbp. We found that 200 of the 566 analysed protein-coding genes were lost in at least one lineage of Blattabacterium, with the most extreme case being one gene that was lost independently in 24 lineages. We found evidence for three mechanisms influencing gene loss in Blattabacterium. First, gene loss rates were found to increase exponentially with the accumulation of substitutions. Second, genes involved in vitamin and amino acid metabolism experienced relaxed selection in Cryptocercus and Mastotermes, possibly triggered by their vertically-inherited gut symbionts. Third, we found evidences of epistatic interactions among genes leading to a ‘domino effect’ of gene loss within pathways. Our results highlight the complexity of the process of genome erosion in an endosymbiont.

Of Cockroaches and Symbionts: Recent Advances in the Characterization of the Relationship between Blattella germanica and Its Dual Symbiotic System

“…On the other hand, and similar to other omnivorous animals, they harbour in their hindgut (the posterior part of the gut) a complex microbiota. The complete genome of at least 70 Blattabacterium strains have been sequenced, and their metabolisms inferred, confirming their monophyletic origin in all cockroaches as well as their essentiality in hosts' physiology [48][49][50][51]. Besides, the gut microbiota has also been characterized in several species, both at taxonomic and functional levels.…”

“…Thus, 200 out of the 566 protein-coding genes under study were lost in at least one lineage, while 25 were lost independently from 10 to 24 times. Such losses affect the genes related to the biosynthesis of amino acids and cofactors to a greater extent, while those involved in nitrogen metabolism are retained [49].…”

Impact of host demography and evolutionary history on endosymbiont molecular evolution: A test in carpenter ants (genusCamponotus) and theirBlochmanniaendosymbionts

“…This is consistent with previous research in Blochmannia endosymbionts identifying lineage‐specific gene loss largely due to relaxed selection constraints and genetic drift (Williams & Wernegreen, 2015 ). Similarly, in cockroach Blattabacterium endosymbionts, Kinjo et al ( 2021 ) found that gene loss was lineage‐specific, and that some genes showed parallel gene loss across multiple Blattabacterium lineages.…”

“…Similarly, in cockroach Blattabacterium endosymbionts, Kinjo et al (2021) found that gene loss was lineage-specific, and that some genes showed parallel gene loss across multiple Blattabacterium lineages.…”

Bacterial cooperation through horizontal gene transfer

“…Strains that stop performing these costly functions and eventually lose the corresponding genes have a local advantage [15]. While gene loss due to drift is known in bacteria, especially in host-restricted taxa [26,27], genome reduction also occurs in bacteria with very large effective population sizes, such as the marine-dwelling Synechococcus and Roseobacter [28,29]. Selective pressure to lose genes could be due to general genome streamlining caused by deletion bias observed in bacterial genomes [30], a possible way to purge them of selfish genetic elements [31].…”