Genome Economization in the Endosymbiont of the Wood Roach Cryptocercus punctulatus Due to Drastic Loss of Amino Acid Synthesis Capabilities

Abstract

Cockroaches (Blattaria: Dictyoptera) harbor the endosymbiont Blattabacterium sp. in their abdominal fat body. This endosymbiont is involved in nitrogen recycling and amino acid provision to its host. In this study, the genome of Blattabacterium sp. of Cryptocercus punctulatus (BCpu) was sequenced and compared with those of the symbionts of Blattella germanica and Periplaneta americana, BBge and BPam, respectively. The BCpu genome consists of a chromosome of 605.7 kb and a plasmid of 3.8 kb and is therefore approximately 31 kb smaller than the other two aforementioned genomes. The size reduction is due to the loss of 55 genes, 23 of which belong to biosynthetic pathways for amino acids. The pathways for the production of tryptophan, leucine, isoleucine/threonine/valine, methionine, and cysteine have been completely lost. Additionally, the genes for the enzymes catalyzing the last steps of arginine and lysine biosynthesis, argH and lysA, were found to be missing and pseudogenized, respectively. These gene losses render BCpu auxotrophic for nine amino acids more than those corresponding to BBge and BPam. BCpu has also lost capacities for sulfate reduction, production of heme groups, as well as genes for several other unlinked metabolic processes, and genes present in BBge and BPam in duplicates. Amino acids and cofactors that are not synthesized by BCpu are either produced in abundance by hindgut microbiota or are provisioned via a copious diet of dampwood colonized by putrefying microbiota, supplying host and Blattabacterium symbiont with the necessary nutrients and thus permitting genome economization of BCpu.

Comparative Genomics of Blattabacterium cuenoti: The Frozen Legacy of an Ancient Endosymbiont Genome

“…Moreover, in termites, a sister clade of cockroaches, only Mastotermes darwiniensis has retained a symbiont (Bandi et al 1995). Recently, another two genomes of Blattabacterium strains have been sequenced from wood-feeding hosts, the subsocial roach Cryptocercus punctulatus (BCpu) (Neef et al 2011), and the termite M. darwiniensis (BMda) (Sabree et al 2012). All these four Blattabacterium genomes show typical features of other insect primary endosymbionts, such as low GC content, total absence of repeated elements, and a reduced genome size compared to their closest free-living relatives (McCutcheon and Moran 2012).…”

“…Moreover, Blattabacterium strains from all four studied species encode urease genes, and endosymbiont-enriched extracts from P. americana and B. germanica show urease activity (López-Sánchez et al 2009), thus this activity may be essential for nitrogen recycling from urate deposits (González-Domenech et al 2012). On the other hand, BCpu and BMda strains retain the enzymes required for nitrogen metabolism, even though they have lost pathways for the synthesis of several amino acids (Neef et al 2011; Sabree et al 2012). …”

Maintenance of essential amino acid synthesis pathways in the Blattabacterium cuenoti symbiont of a wood-feeding cockroach

“…BPAA are most similar to those of related strains from nonwood-feeding hosts, rather than other wood-feeding hosts (figure 1). In strains CPU and MADAR, genes encoding pathways for the production of six of ten EAAs are absent, with one additional pathway (lysine) being interrupted [6,10]. Str.…”

“…Gene content in str. BPAA's genome is highly similar to that in other B. cuenoti genomes (see the electronic supplementary material), suggesting their last common ancestor had a highly reduced genome [6][7][8][9][10]. Phylogenetic analysis placed strains BPAA and BGIGA as sister groups, distant from strains CPU and MADAR (see figure 1 and electronic supplementary material).…”

“…The first assumes that their ancestral host fed on decaying wood similar to that which C. punctulatus now feeds on. Because decaying wood contains a complex microbiota, digestion and assimilation of microbes in the ancestral host may have provided the host with all EAAs, leading to relaxed selection on the maintenance of EAA pathways in B. cuenoti [6]. The second hypothesis proposes that the ancestral host developed a hindgut microbiota that supplanted many of the functions of B. cuenoti, again leading to relaxed selection on EAA pathways [6,10].…”