Academic journal article Genetics

Decoupling of Host-Symbiont-Phage Coadaptations Following Transfer between Insect Species

Academic journal article Genetics

Decoupling of Host-Symbiont-Phage Coadaptations Following Transfer between Insect Species

Article excerpt

ABSTRACT

Transferring endosymbiotic bacteria between different host species can perturb the coordinated regulation of the host and bacterial genomes. Here we use the most common maternally transmitted bacteria, Wolbachia pipientis, to test the consequences of host genetic background on infection densities and the processes underlying those changes in the parasitoid wasp genus Nasonia. Introgressing the genome of Nasonia giraulti into the infected cytoplasm of N. vitripennis causes a two-order-of-magnitude increase in bacterial loads in adults and a proliferation of the infection to somatic tissues. The host effect on W. pipientis distribution and densities is associated with a twofold decrease in densities of the temperate phage WO-B. Returning the bacteria from the new host species back to the resident host species restores the bacteria and phage to their native densities. To our knowledge, this is the first study to report a host-microbe genetic interaction that affects the densities of both W. pipientis and bacteriophage WO-B. The consequences of the increased bacterial density include a reduction in fecundity, an increase in levels of cytoplasmic incompatibility (CI), and unexpectedly, male-to-female transfer of the bacteria to uninfected females and an increased acceptance of densely infected females to interspecific mates. While paternal inheritance of the W. pipientis was not observed, the high incidence of male-to-female transfer in the introgressed background raises the possibility that paternal transmission could be more likely in hybrids where paternal leakage of other cytoplasmic elements is also known to occur. Taken together, these results establish a major change in W. pipientis densities and tissue tropism between closely related species and support a model in which phage WO, Wolbachia, and arthropods form a tripartite symbiotic association in which all three are integral to understanding the biology of this widespread endosymbiosis.

ALL metazoans are populated by symbiotic bacteria, some of which live in intimate association with their hosts as maternally transmitted infections. Wolbachia pipientis is one of the most prevalent species of bacterial endosymbionts in the animal world that exemplifies this lifestyle. It is maternally transmitted from host ovaries to developing eggs in filarial nematodes and arthropods. In filarial nematodes, W. pipientis are obligate mutualists (Taylor et al. 2005) and assist fertility (Hoerauf et al. 1999) and larval development (Smith and Rajan 2000). Proinflammatory responses in filarial-infected vertebrates indicate that the endosymbiont rather than the nematode is the significant contributor to the acute pathologies of human river blindness (Saint Andre et al. 2002) and elephantiasis (Taylor et al. 2000). In arthropods, W. pipientis are reproductive parasites (Stouthamer et al. 1999; Werren et al. 2008) and, less often, mutualists (Pannebakker et al. 2007; Hosokawa et al. 2010), and occur in~66% of all insect species worldwide (Hilgenboecker et al. 2008). Thus, millions of animal species are infected byW. pipientis and over 1 billion people in ≥80 countries are at risk of filarial/W. pipientis diseases (Ottesen et al. 2008). As one of the great pandemics in the animal world, W. pipientis offer a preeminent model to explore the varied outcomes of infection between animal cells and obligate intracellular bacteria.

Transfer of symbionts between closely related species is a useful tool to determine the role of host genes in regulating a symbiosis. Over time, maternally inherited bacteria may coevolve with their hosts to finely tune their densities, tissue tropism, and interactions with host fitness. Many studies have found that relocating W. pipientis to a new host species causes changes in reproductive parasitism, bacterial titers, and tissue distribution not observed in the donor (Boyle et al. 1993; Bordenstein and Werren 1998; McGraw et al. 2002; Riegler et al. …

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