Diversifying selection and host adaptation in two endosymbiont genomes

School of Integrative Biology, University of Queensland, Brisbane, QLD, Australia. <>
BMC Evolutionary Biology (Impact Factor: 3.37). 02/2007; 7(1):68. DOI: 10.1186/1471-2148-7-68
Source: PubMed


The endosymbiont Wolbachia pipientis infects a broad range of arthropod and filarial nematode hosts. These diverse associations form an attractive model for understanding host:symbiont coevolution. Wolbachia's ubiquity and ability to dramatically alter host reproductive biology also form the foundation of research strategies aimed at controlling insect pests and vector-borne disease. The Wolbachia strains that infect nematodes are phylogenetically distinct, strictly vertically transmitted, and required by their hosts for growth and reproduction. Insects in contrast form more fluid associations with Wolbachia. In these taxa, host populations are most often polymorphic for infection, horizontal transmission occurs between distantly related hosts, and direct fitness effects on hosts are mild. Despite extensive interest in the Wolbachia system for many years, relatively little is known about the molecular mechanisms that mediate its varied interactions with different hosts. We have compared the genomes of the Wolbachia that infect Drosophila melanogaster, wMel and the nematode Brugia malayi, wBm to that of an outgroup Anaplasma marginale to identify genes that have experienced diversifying selection in the Wolbachia lineages. The goal of the study was to identify likely molecular mechanisms of the symbiosis and to understand the nature of the diverse association across different hosts.
The prevalence of selection was far greater in wMel than wBm. Genes contributing to DNA metabolism, cofactor biosynthesis, and secretion were positively selected in both lineages. In wMel there was a greater emphasis on DNA repair, cell division, protein stability, and cell envelope synthesis.
Secretion pathways and outer surface protein encoding genes are highly affected by selection in keeping with host:parasite theory. If evidence of selection on various cofactor molecules reflects possible provisioning, then both insect as well as nematode Wolbachia may be providing substances to hosts. Selection on cell envelope synthesis, DNA replication and repair machinery, heat shock, and two component switching suggest strategies insect Wolbachia may employ to cope with diverse host and intra-host environments.

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    • "For pathogens, both diversifying (positive) selection [26,27] and purifying (negative) selection [28,29] have been reported. The situation in symbionts has not been extensively studied, except for few brief reports on Wolbachia or Rhizobium[30,31]. We undertook this investigation on genomes of three important but diverse genera of Actinobacteria to analyze the selection pressures working on them and have also looked into the evolutionary rate of secreted proteins to assess their biochemical adaptations to the environment. "
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    • "Their presence is revealed through PCR detection, or upon transfection experiments (the haemolymph proves infectious) [43]–[46]. They are believed to remain extracellular in the plasma [50], especially since Rasgon et al. [51] showed they can survive outside cells. Wolbachia are observed inside haemocytes only in the crustacean A. vulgare [28], [30]. "
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    ABSTRACT: Most of crustacean immune responses are well described for the aquatic forms whereas almost nothing is known for the isopods that evolved a terrestrial lifestyle. The latter are also infected at a high prevalence with Wolbachia, an endosymbiotic bacterium which affects the host immune system, possibly to improve its transmission. In contrast with insect models, the isopod Armadillidium vulgare is known to harbor Wolbachia inside the haemocytes. In A. vulgare we characterized three haemocyte types (TEM, flow cytometry): the hyaline and semi-granular haemocytes were phagocytes, while semi-granular and granular haemocytes performed encapsulation. They were produced in the haematopoietic organs, from central stem cells, maturing as they moved toward the edge (TEM). In infected individuals, live Wolbachia (FISH) colonized 38% of the haemocytes but with low, variable densities (6.45±0.46 Wolbachia on average). So far they were not found in hyaline haemocytes (TEM). The haematopoietic organs contained 7.6±0.7×10(3)Wolbachia, both in stem cells and differentiating cells (FISH). While infected and uninfected one-year-old individuals had the same haemocyte density, in infected animals the proportion of granular haemocytes in particular decreased by one third (flow cytometry, Pearson's test = 12 822.98, df = 2, p<0.001). The characteristics of the isopod immune system fell within the range of those known from aquatic crustaceans. The colonization of the haemocytes by Wolbachia seemed to stand from the haematopoietic organs, which may act as a reservoir to discharge Wolbachia in the haemolymph, a known route for horizontal transfer. Wolbachia infection did not affect the haemocyte density, but the quantity of granular haemocytes decreased by one third. This may account for the reduced prophenoloxidase activity observed previously in these animals.
    PLoS ONE 04/2011; 6(4):e18531. DOI:10.1371/journal.pone.0018531 · 3.23 Impact Factor
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    • "This observation is not unprecedented as evidence of endosymbiont genomes (e.g. Wolbachia) undergoing either purifying or diversifying selection when examined from different host species has also been described with cell envelope component genes (Brownlie et al. 2007). "
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