Dataset Information

Infection dynamics of coexisting beta- and gammaproteobacteria in the nested endosymbiotic system of mealybugs.

ABSTRACT: We investigated the infection dynamics of endosymbiotic bacteria in the developmental course of the mealybugs Planococcus kraunhiae and Pseudococcus comstocki. Molecular phylogenetic analyses identified a betaproteobacterium and a gammaproteobacterium from each of the mealybug species. The former bacterium was related to the beta-endosymbionts of other mealybugs, i.e., "Candidatus Tremblaya princeps," and formed a compact clade in the Betaproteobacteria. Meanwhile, the latter bacterium was related to the gamma-endosymbionts of other mealybugs but belonged to distinct clades in the Gammaproteobacteria. Whole-mount in situ hybridization confirmed the peculiar nested formation in the endosymbiotic system of the mealybugs: the beta-endosymbiont cells were present in the cytoplasm of the bacteriocytes, and the gamma-endosymbiont cells were located in the beta-endosymbiont cells. In nymphal and female development, a large oval bacteriome consisting of a number of bacteriocytes was present in the abdomen, wherein the endosymbionts were harbored. In male development, strikingly, the bacteriome progressively degenerated in prepupae and pupae and became almost unrecognizable in adult males. In the degeneration process, the gamma-endosymbionts disappeared more rapidly than the beta-endosymbionts did. Quantitative PCR analyses revealed that (i) the population dynamics of the endosymbionts in female development reflected the reproductive activity of the insects, (ii) the population dynamics of the endosymbionts were strikingly different between female development and male development, (iii) the endosymbiont populations drastically decreased in male development, and (iv) the gamma-endosymbiont populations decreased more rapidly than the beta-endosymbiont populations in male development. Possible mechanisms underlying the uncoupled regulation of the beta- and gamma-endosymbiont populations are discussed in relation to the establishment and evolution of this unique prokaryote-prokaryote endosymbiotic system.

SUBMITTER: Kono M

PROVIDER: S-EPMC2446506 | biostudies-literature | 2008 Jul

REPOSITORIES: biostudies-literature

ACCESS DATA

Publications

Infection dynamics of coexisting beta- and gammaproteobacteria in the nested endosymbiotic system of mealybugs.

Kono Marie M Koga Ryuichi R Shimada Masakazu M Fukatsu Takema T

Applied and environmental microbiology 20080509 13

We investigated the infection dynamics of endosymbiotic bacteria in the developmental course of the mealybugs Planococcus kraunhiae and Pseudococcus comstocki. Molecular phylogenetic analyses identified a betaproteobacterium and a gammaproteobacterium from each of the mealybug species. The former bacterium was related to the beta-endosymbionts of other mealybugs, i.e., "Candidatus Tremblaya princeps," and formed a compact clade in the Betaproteobacteria. Meanwhile, the latter bacterium was relat ...[more]

PMID: 18469124

Similar Datasets

Project description:Bacteria rapidly adapt to their environment by integrating external stimuli through diverse signal transduction systems. Pseudomonas aeruginosa, for example, senses surface contact through the Wsp signal transduction system to trigger the production of cyclic di-GMP. Diverse mutations in wsp genes that manifest enhanced biofilm formation are frequently reported in clinical isolates of P. aeruginosa and in biofilm studies of Pseudomonas spp. and Burkholderia cenocepacia. In contrast to the convergent phenotypes associated with comparable wsp mutations, we demonstrate that the Wsp system in B. cenocepacia does not impact intracellular cyclic di-GMP levels, unlike that in Pseudomonas spp. Our current mechanistic understanding of the Wsp system is based entirely on the study of four Pseudomonas spp., and its phylogenetic distribution remains unknown. Here, we present a broad phylogenetic analysis to show that the Wsp system originated in the betaproteobacteria and then horizontally transferred to Pseudomonas spp., the sole member of the gammaproteobacteria. Alignment of 794 independent Wsp systems with reported mutations from the literature identified key amino acid residues that fall within and outside annotated functional domains. Specific residues that are highly conserved but uniquely modified in B. cenocepacia likely define mechanistic differences among Wsp systems. We also find the greatest sequence variation in the extracellular sensory domain of WspA, indicating potential adaptations to diverse external stimuli beyond surface contact sensing. This study emphasizes the need to better understand the breadth of functional diversity of the Wsp system as a major regulator of bacterial adaptation beyond B. cenocepacia and select Pseudomonas spp. IMPORTANCE The Wsp signal transduction system serves as an important model system for studying how bacteria adapt to living in densely structured communities known as biofilms. Biofilms frequently cause chronic infections and environmental fouling, and they are very difficult to eradicate. In Pseudomonas aeruginosa, the Wsp system senses contact with a surface, which in turn activates specific genes that promote biofilm formation. We demonstrate that the Wsp system in Burkholderia cenocepacia regulates biofilm formation uniquely from that in Pseudomonas species. Furthermore, a broad phylogenetic analysis reveals the presence of the Wsp system in diverse bacterial species, and sequence analyses of 794 independent systems suggest that the core signaling components function similarly but with key differences that may alter what or how they sense. This study shows that Wsp systems are highly conserved and more broadly distributed than previously thought, and their unique differences likely reflect adaptations to distinct environments.

Dataset Information

Infection dynamics of coexisting beta- and gammaproteobacteria in the nested endosymbiotic system of mealybugs.

Publications

Infection dynamics of coexisting beta- and gammaproteobacteria in the nested endosymbiotic system of mealybugs.

Similar Datasets

OmicsDI is part of the ELIXIR infrastructure

Tweets