Wolbachia density and virulence attenuation after transfer into a novel host

Yale University, New Haven, Connecticut, United States
Proceedings of the National Academy of Sciences (Impact Factor: 9.67). 04/2002; 99(5):2918-23. DOI: 10.1073/pnas.052466499
Source: PubMed


The factors that control replication rate of the intracellular bacterium Wolbachia pipientis in its insect hosts are unknown and difficult to explore, given the complex interaction of symbiont and host genotypes. Using a strain of Wolbachia that is known to over-replicate and shorten the lifespan of its Drosophila melanogaster host, we have tracked the evolution of replication control in both somatic and reproductive tissues in a novel host/Wolbachia association. After transinfection (the transfer of a Wolbachia strain into a different species) of the over-replicating Wolbachia popcorn strain from D. melanogaster to Drosophila simulans, we demonstrated that initial high densities in the ovaries were in excess of what was required for perfect maternal transmission, and were likely causing reductions in reproductive fitness. Both densities and fitness costs associated with ovary infection rapidly declined in the generations after transinfection. The early death effect in D. simulans attenuated only slightly and was comparable to that induced in D. melanogaster. This study reveals a strong host involvement in Wolbachia replication rates, the independence of density control responses in different tissues, and the strength of natural selection acting on reproductive fitness.

Download full-text


Available from: David J Merritt
  • Source
    • "Yet it is not understood how well-known symbioses such as between leafcutter ants and fungi (Mueller et al. 2005; Schultz and Brady 2008), fig wasps and trees (Machado et al. 2001; Herre et al. 2008) or humans and their microbiota (Human Microbiome Project Consortium 2012) originated. Insights are traditionally inferred from comparative studies on closely related species groups such as Wolbachia, which shows the full spectrum of symbiosis, including parasitism, where one partner receives fitness benefits at the expense of the other, commensalism, which brings asymmetrical advantage to one partner at no cost to the other, and mutualism, which favors both (McGraw et al. 2002; Fry et al. 2004). Nevertheless, empirical evidence for the origin of symbiosis remains equivocal because confounding factors in the history of these associations cannot be excluded and, therefore, cause and effect relationships cannot easily be teased apart. "
    [Show abstract] [Hide abstract]
    ABSTRACT: Symbiotic interactions are indispensable for metazoan function, but their origin and evolution remains elusive. We use a controlled evolution experiment to demonstrate the emergence of novel commensal interactions between Pseudomonas aeruginosa, an initially pathogenic bacterium, and a metazoan host, C. elegans. We show that commensalism evolves through loss of virulence, because it provides bacteria with a double fitness advantage: increased within-host fitness and a larger host population to infect. Commensalism arises irrespective of host immune status, as the adaptive path in immunocompromised C. elegans knock-outs does not differ from that in wild type. Dissection of temporal dynamics of genomic adaptation for 125 bacterial populations reveals highly parallel evolution of incipient commensalism across independent biological replicates. Adaptation is mainly achieved through frame shift mutations in the global regulator lasR and non-synonymous point mutations in the polymerase gene rpoB that arise early in evolution. Genetic knock-outs of lasR corroborate its role in virulence attenuation, but also show that further mutations are necessary for the fully commensal phenotype. The evolutionary transition from pathogenicity to commensalism as we observe here is facilitated by mutations in global regulators such as lasR, because few genetic changes cause pleiotropic effects across the genome with large phenotypic effects. Finally, we found that nucleotide diversity increased more quickly in bacteria adapting to immunocompromised hosts than in those adapting to immunocompetent hosts. Nevertheless, the outcome of evolution was comparable across host types. Commensalism can thus evolve independently of host immune state solely as a side-effect of bacterial adaptation to novel hosts. © The Author(s) 2015. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution.
    Full-text · Article · Jul 2015 · Molecular Biology and Evolution
  • Source
    • "A second, and not mutually exclusive hypothesis, is that rapid adaptation of symbionts to novel host environments permits long-term persistence of symbionts whose initial performance in a host is poor. Indeed, several studies have shown attenuated direct costs to the fitness of the host over time in the virulent 'popcorn' strain of Wolbachia (McGraw et al., 2002; Carrington et al., 2010), as well as evolution towards mutualism of strains in nature (Weeks et al., 2007). The genus Spiroplasma is one of the most common maternally inherited endosymbiont groups, with a wide range of hosts including insects, crustaceans, arachnids and plants (Gasparich et al., 2004). "
    [Show abstract] [Hide abstract]
    ABSTRACT: Maternally inherited symbionts are common in arthropods and many have important roles in host adaptation. The observation that specific symbiont lineages infect distantly related host species implies new interactions are commonly established by lateral transfer events. However, studies have shown that symbionts often perform poorly in novel hosts. We hypothesized selection on the symbiont may be sufficiently rapid that poor performance in a novel host environment is rapidly ameliorated, permitting symbiont maintenance. Here, we test this prediction for a Spiroplasma strain transinfected into the novel host Drosophila melanogaster. In the generations immediately following transinfection, the symbiont had low transmission efficiency to offspring and imposed severe fitness costs on its host. We observed that effects on host fitness evolved rapidly, being undetectable after 17 generations in the novel host, whereas vertical transmission efficiency was poorly responsive over this period. Our results suggest that long-term symbiosis may more readily be established in cases where symbionts perform poorly in just one aspect of symbiosis.Heredity advance online publication, 4 February 2015; doi:10.1038/hdy.2014.112.
    Full-text · Article · Feb 2015 · Heredity
  • Source
    • "The exponential growth of the symbiont may be the cause of the life-shortening, either by direct tissue damage or by constituting a significant metabolic burden compromising the insect's health. This is reminiscent of host life-shortening by the exponentially growing wMelPop strain [15], [17], [44]. "
    [Show abstract] [Hide abstract]
    ABSTRACT: Wolbachia, endosymbionts that reside naturally in up to 40-70% of all insect species, are some of the most prevalent intracellular bacteria. Both Wolbachia wAu, naturally associated with Drosophila simulans, and wMel, native to Drosophila melanogaster, have been previously described to protect their hosts against viral infections. wMel transferred to D. simulans was also shown to have a strong antiviral effect. Here we directly compare one of the most protective wMel variants and wAu in D. melanogaster in the same host genetic background. We conclude that wAu protects better against viral infections, it grows exponentially and significantly shortens the lifespan of D. melanogaster. However, there is no difference between wMel and wAu in the expression of selected antimicrobial peptides. Therefore, neither the difference in anti-viral effect nor the life-shortening could be attributed to the immune stimulation by exogenous Wolbachia. Overall, we prove that stable transinfection with a highly protective Wolbachia is not necessarily associated with general immune activation.
    Full-text · Article · Jun 2014 · PLoS ONE
Show more