Host tissues as microhabitats for Wolbachia and quantitative insights into the bacterial community in terrestrial isopods

Abstract

Animal-bacterial symbioses are highly dynamic in terms of multipartite interactions, both between the host and its symbionts as well as between the different bacteria constituting the symbiotic community. These interactions will be reflected by the titres of the individual bacterial taxa, for example via host regulation of bacterial loads or competition for resources between symbionts. Moreover, different host tissues represent heterogeneous microhabitats for bacteria, meaning that host-associated bacteria might establish tissue-specific bacterial communities. Wolbachia are widespread endosymbiotic bacteria, infecting a large number of arthropods and filarial nematodes. However, relatively little is known regarding direct interactions between Wolbachia and other bacteria. This study represents the first quantitative investigation of tissue-specific Wolbachia-microbiota interactions in the terrestrial isopod Armadillidium vulgare. To this end, we obtained a more complete picture of the Wolbachia distribution patterns across all major host tissues, integrating all three feminizing Wolbachia strains (wVulM, wVulC, wVulP) identified to date in this host. Interestingly, the different Wolbachia strains exhibited strain-specific tissue distribution patterns, with wVulM reaching lower titres in most tissues. These patterns were consistent across different host genetic backgrounds and might reflect different co-evolutionary histories between the Wolbachia strains and A. vulgare. Moreover, Wolbachia-infected females carried higher total bacterial loads in several, but not all, tissues, irrespective of the Wolbachia strain. Taken together, this quantitative approach indicates that Wolbachia is part of a potentially more diverse bacterial community, as exemplified by the presence of highly abundant bacterial taxa in the midgut caeca of several A. vulgare populations.

Symbiotic Bacteria Influence the Odor and Mating Preference of Their Hosts

“…Numerous studies have highlighted the complexity of the symbiotic bacteria Wolbachia, in terms of its impact on its host's reproductive organs and somatic tissues (Miller and Schneider, 2012) and its accumulation in the nervous system (Strunov et al, 2013;Dittmer et al, 2014). Wolbachia are one of the most prevalent gram-negative bacteria in arthropods (Werren and Windsor, 2000;Hilgenboecker et al, 2008;Serbus et al, 2008;Cordaux et al, 2012).…”

Host, Symbionts, and the Microbiome: The Missing Tripartite Interaction

“…Competition for resources or space between Wolbachia and other bacteria is also likely for the terrestrial isopod Armadillidium vulgare. In this pill bug, total bacterial loads increase in some, but not all, tissues of Wolbachiainfected individuals [20], and the presence of Wolbachia decreases the abundance of bacterial phylotypes [21]. The nutritional mutualism in the bed bug Cimex lectularius is an other example for direct interactions.…”

A host as an ecosystem:Wolbachiacoping with environmental constraints

“…Indeed, the Wolbachia have been observed in virtually all major organs including the brain, nerve cord, muscles, fat body, Malpighian tubules, salivary glands, gnathosoma, haemolymph and midgut in insects, mites and crustaceans (e.g. Min and Benzer, ; Dobson et al ., ; Ijichi et al ., ; Goto et al ., ; Narita et al ., 2007a; Zouache et al ., ; Andersen et al ., ; Osborne et al ., ; Zhao et al ., ; Dittmer et al ., ; Fig. ).…”

“…In this context, recent findings from terrestrial isopods indicate that (i) Wolbachia densities vary across host tissues in naturally single‐infected individuals (e.g. Dittmer et al ., ) and (ii) Wolbachia proliferation in transinfected individuals differs depending on the source tissue of the transferred bacteria (Le Clec'h et al ., ).…”