Symbiotic bacteria in hepatopancreas (midgut glands) of isopods (Crustacea: Isopoda) : phylogeny, evolution, and distribution

Wang, Yongjie

Terrestrial isopods harbor uncultured bacterial symbionts in their midgut glands (hepatopancreas) that may have facilitated the evolutionary shift to utilizing terrestrial leaf litter during the course of colonizing land. In a first molecular-biological approach, we screened isopods from marine, semi-terrestrial, terrestrial, and freshwater habitats for hepatopancreatic bacterial symbionts by means of 16S rRNA gene cloning and sequencing, denaturing gel gradient electrophoresis (DGGE), fluorescence-labeled specific oligonucleotide probe in situ hybridization (FISH), and electron microscopy. There are no hepatopancreatic bacteria in the marine isopod Idotea balthica, while high numbers of nearly uniform morphotypes of bacteria were detected in semi-terrestrial (Ligia oceanica), terrestrial (Porcellio scaber, Oniscus asellus, Philoscia muscorum, Armadilidium vulgare, Trachelipus rathkii, and Alloniscs perconvesus), and freshwater (Asellus aquaticus) isopods. Phylogenetic analyses demonstrated that the symbiotic bacteria in this three types of isopod species are not closely related but belong to bacterial taxa as different as Pseudomonas (g-Proteobacteria, similarity >98%) in L. oceanica, Rickettsiales (a-Proteobacteria, similarity <81%) and Mycoplasmatales (Mollicutes, similarity <82%) in P. scaber and O. asellus, and Rhodobacter (a-Proteobacteria, similarity >95%), Burkholderia (b-Proteobacteria, similarity >98%), Aeromonas (g-Proteobacteria, similarity >99%) and Rickettsiella (g-Proteobacteria, similarity >96%) in A. aquaticus, respectively. These findings suggest that hepatopancreatic symbionts either have been acquired several times independently or have been exchanged during isopod evolution. Rickettsia-like and Mycoplasma-like symbionts of terrestrial isopod represent prevalent symbionts in several geographically distinct isopod populations. These results suggest either a common ancestor of terrestrial isopod that already harboured these bacteria symbionts or horizontal inter-specific transmission of the symbionts. Based on FISH and diagnostic PCR techniques, our data suggest that the Mycoplasma-like hepatopancreatic symbionts of P. scaber are environmentally transmitted to the new progeny exposing to the external environment. Except for the g-Proteobacteria and b-Proteobacteria found in L. oceanica and A. aquaticus, respectively, close relatives of isopod symbionts are not known to produce any enzyme that might facilitate the digestion of leaf litter, suggesting that the proposed contribution of bacterial symbionts to digestive processes of isopod hosts is unlikely.



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Wang, Yongjie: Symbiotic bacteria in hepatopancreas (midgut glands) of isopods (Crustacea: Isopoda) : phylogeny, evolution, and distribution. 2004.


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