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

Abstract

In addition to harbouring intestinal symbionts, some animal species also possess intracellular symbiotic microbes. The relative contributions of gut-resident and intracellular symbionts to host metabolism, and how they coevolve are not well understood. Cockroaches and the termite Mastotermes darwiniensis present a unique opportunity to examine the evolution of spatially separated symbionts, as they harbour gut symbionts and the intracellular symbiont Blattabacterium cuenoti. The genomes of B. cuenoti from M. darwiniensis and the social wood-feeding cockroach Cryptocercus punctulatus are each missing most of the pathways for the synthesis of essential amino acids found in the genomes of relatives from non-wood-feeding hosts. Hypotheses to explain this pathway degradation include: (i) feeding on microbes present in rotting wood by ancestral hosts; (ii) the evolution of high-fidelity transfer of gut microbes via social behaviour. To test these hypotheses, we sequenced the B. cuenoti genome of a third wood-feeding species, the phylogenetically distant and non-social Panesthia angustipennis. We show that host wood-feeding does not necessarily lead to degradation of essential amino acid synthesis pathways in B. cuenoti, and argue that ancestral high-fidelity transfer of gut microbes best explains their loss in strains from M. darwiniensis and C. punctulatus.

Multiorganismal Insects: Diversity and Function of Resident Microorganisms

“…Microbial involvement in essential amino acid provisioning in other plant sap–feeding insects is indicated by the apparently universal incidence of symbioses in these insects (16) and by the retention of essential amino acid biosynthesis genes in all symbionts tested (76). Microbial symbionts have also been implicated in essential amino acid provisioning in ants (45), cockroaches (95), and some wood roaches (113). …”

Food availability affects the strength of mutualistic host–microbiota interactions in Daphnia magna

“…It is well known that the gut microbiota can have a positive impact on the fitness of its host through various mechanisms like producing essential nutrients (Tokuda et al, 2013), enhancing resistance to disease (Belden & Harris, 2007) or breaking down indigestible substances (Ohkuma, 2008) and toxic compounds (Kohl & Dearing, 2012). In some cases, however, host fitness can also be reduced by the microbiota through competition for resources (Douglas, 2010) or via a dysfunctional symbiotic microbial community causing disease (Clemente et al, 2012).…”

The cockroachBlattella germanicaobtains nitrogen from uric acid through a metabolic pathway shared with its bacterial endosymbiont

“…urate oxidase, allantoinase and allantoicase) and also the supply of non-essential amino acids to the endosymbiont. Despite the presence of many of these enzymes among Bacteroidetes [8], none of the Blattabacterium genomes sequenced so far contains the necessary genes [10,11]. However, urate oxidase activity was detected in some tissues of the cockroaches Leucophaea maderae [12] and P. americana [13].…”