The taxophysiological paradox: changes in the intestinal microbiota of the xylophagous cockroach Cryptocercus punctulatus depending on the physiological state of the host

Abstract

The phylogenetic relationships of symbiotic bacteria from the xylophagous cockroach Cryptocercus (Cryptocercidae, Blattaria) were compared to those described in previous reports in lower termites. The 16S rDNA bacterial genes were PCR-amplified from DNA isolated from the entire hindgut using Bacteria-selective primers, and the 16S rDNA amplicons were cloned into Escherichia coli. The changes in the gut microbiota of Cryptocercus under three physiological conditions, “active,” “fasting,” and “dead,” were studied. Analysis of the active-clone library revealed 45 new phylotypes (clones sharing > 97% sequence identity were grouped into the same phylotype) from 54 analyzed clones. The clones were affiliated with the phyla Firmicutes, Bacteroidetes, Proteobacteria, Actinobacteria, Spirochaetes, Synergistetes, Verrucomicrobia, and candidate phylum Termite Group 1 (TG1). Clones belonging to Spirochaetes, Bacteroidetes, and TG1 phyla clustered with previously reported sequences obtained from the guts of several termites, suggesting that these clones are common constituents of the intestinal microbiota of lower termites and Cryptocercus. In the fasting-clone library, 19 new phylotypes, from 49 clones studied, were distinguished. The new phylotypes were affiliated with the phyla Bacteroidetes, Firmicutes, Actinobacteria, Proteobacteria, Spirochaetes, Synergistetes, and the candidate phylum TM7. Finally, in the dead-clone library, 24 new phylotypes from 50 studied clones were found. The new phylotypes were affiliated with the phyla Firmicutes, Actinobacteria, and Proteobacteria. Thus, from active, to fasting, to dead physiological states, a decrease in the number of phyla present in the whole microbial gut was evident. However, in the dead physiological state, each phylum conserved contained more new phylotypes. This poses a taxophysiological paradox, because a stable, active physiological state of Cryptocercus—due to a continuous input of wood—supports a higher diversity of bacterial phyla, probably necessary to maintain a sharp O₂–H₂ gradient in the gut. By contrast, in the dead state, nutrient input is limited to the residual gut microbiota that is killed by the newly oxic environment, thus providing a food source for other, aerobic or facultative anaerobic bacteria. This results in an increase in the internal diversity of the few remaining phyla. [Int Microbiol 2009; 12(4):227-236]