The bacterial community in the guts of the oriental, Blaberidae cockroaches Opisthoplatia orientalis

Abstract

Microbial symbiosis in the guts of animals helps food digestion, nutrients assimilation and many other important aspects of physiology. Most of the guts in animals are colonized with a consortium of microbes which have been described as another vital organ to animals. Symbiosis is a dynamic interaction susceptible to both endogenous and exogenous factors, resulting in a shift of the microbial community structure together with host physiological responses. Although some studies have suggested that host phylogeny and environment would help to shape the host gut microbiota, their influence has not been extensively substantiated in different lab models.

Opisthoplatia orientalis (Order Blattodea, Family Blaberidae) are omnivorous and amphibious cockroaches that only reside in the wild. They feed on leaf litter, flowers as well as decaying materials. Recently, massive appearance of this species were found around Shirahama of Japan. Their unprecedented invasion may lead to a problem of pathogens transmission. Studying if host phylogeny and environment are factors to shape the insects' gut microbiota with O. orientalis as a model will be favorable.

Individuals of O. orientalis were collected in the Nature Reserves of Hong Kong for the study of the natural gut microbial community of this wild species. Large-scale phylogenetic analysis based on bacterial 16S rRNA gene showed that phylotypes in O. orientalis closely clustered with other cockroaches and termites species. Hence, this suggests that phylogenetically-relevant insects share similar gut microbiota.

Comparative study of the gut microbial community was performed between individuals of O. orientalis from invaded human habitats of Japan and also from forests of Hong Kong. Invasive species in Japan revealed increases in both microbial richness and diversity of the invasive species. Interestingly, we observed the disappearance of insect-core microbes for example Clostridium, Citrobacter and Pantoea in the guts of wild individuals which possibly impaired the digestion of cellulosic plant materials, nitrogen fixation and recycling of nitrogenous waste in hosts. Consequently, such disappearance can cause detrimental effect to the host adaptation to new habitats. However, human-associated microbes including Anaeroplasma, Anaerovorax and Parabacteroides were identified in the invasive species which were likely obtained from the human habitats. Such microbial acquisition possibly compensated for the lost functions and caused host adaptation to new habitats.

Collectively, this study demonstrated that 1) host phylogeny does play a role in shaping gut microbiota. 2) Environment is a factor in shaping the structure of insects' gut microbial community and helping hosts to survive in new habitats. Our findings allow us to better understand the insect-microbes symbiosis.