The Terrestrial Isopod Microbiome: An All-in-One Toolbox for Animal-Microbe Interactions of Ecological Relevance

Abstract

Bacterial symbionts represent essential drivers of arthropod ecology and evolution, influencing host traits such as nutrition, reproduction, immunity, and speciation. However, the majority of work on arthropod microbiota has been conducted in insects and more studies in non-model species across different ecological niches will be needed to complete our understanding of host-microbiota interactions. In this review, we present terrestrial isopod crustaceans as an emerging model organism to investigate symbiotic associations with potential relevance to ecosystem functioning. Terrestrial isopods comprise a group of crustaceans that have evolved a terrestrial lifestyle and represent keystone species in terrestrial ecosystems, contributing to the decomposition of organic matter and regulating the microbial food web. Since their nutrition is based on plant detritus, it has long been suspected that bacterial symbionts located in the digestive tissues might play an important role in host nutrition via the provisioning of digestive enzymes, thereby enabling the utilization of recalcitrant food compounds (e.g., cellulose or lignins). If this were the case, then (i) the acquisition of these bacteria might have been an important evolutionary prerequisite for the colonization of land by isopods, and (ii) these bacterial symbionts would directly mediate the role of their hosts in ecosystem functioning. Several bacterial symbionts have indeed been discovered in the midgut caeca of terrestrial isopods and some of them might be specific to this group of animals (i.e., Candidatus Hepatoplasma crinochetorum, Candidatus Hepatincola porcellionum, and Rhabdochlamydia porcellionis), while others are well-known intracellular pathogens (Rickettsiella spp.) or reproductive parasites (Wolbachia sp.). Moreover, a recent investigation of the microbiota in Armadillidium vulgare has revealed that this species harbors a highly diverse bacterial community which varies between host populations, suggesting an important share of environmental microbes in the host-associated microbiota. In this review, we synthesize our current knowledge on the terrestrial isopod microbiome and identify future directions to (i) fully understand the functional roles of particular bacteria (both intracellular or intestinal symbionts and environmental gut passengers), and (ii) whether and how the host-associated microbiota could influence the performance of terrestrial isopods as keystone species in soil ecosystems.

Keywords: bacterial diversity; ecological interactions; endosymbionts; microbiota; symbiosis; terrestrial isopods.

FIGURE 1

Diversity of terrestrial isopods from littoral to desert habitats. (A) The semi-terrestrial Tylos europaeus, inhabiting the littoral zone; (B) the freshwater isopod Asellus aquaticus; (C) the common woodlouse Oniscus asellus; (D) the rough woodlouse Porcellio scaber; (E) the pillbug Armadillidum vulgare during mating; (F) the “zebra pillbug” Armadillidium maculatum; (G) the desert isopod Hemilepistus reaumuri near the entrance of a burrow in Tunisia; and (H) the ant woodlouse Platyarthrus hoffmannseggii. This species is blind and lives in ant nests. Picture credit: Martin Zimmer (B), Sören Franzenburg (D), Giuseppe Montesanto (G), UMR CNRS 7267 (A,C,E,F,H).

FIGURE 2

TEM of Wolbachia in the nerve cord of A. vulgare. W = Wolbachia. Scale bar: 1 μm. Picture credit: Maryline Raimond.

FIGURE 3

(A) SEM of Rickettsiella in the hemolymph of P. scaber. (B) TEM of Rickettsiella in an ovary of Atlantoscia floridana, showing bacterial cells of two different stages: rod-shaped Elementary Bodies (black arrowheads) and replicative Reticulate Bodies (white arrowheads). Scale bar: 1 μm. Picture credit: Maryline Raimond (A,B) and Bianca Lais Zimmermann (B).

FIGURE 4

TEM of Hepatoplasma(A) and Hepatincola(B) in the lumen of the hepatopancreas (midgut glands) of P. scaber. Note how both bacteria attach to the microvillous border of the host cell via stalk-like appendages. Scale bars: 1 μm. Picture credit: Yongjie Wang.

FIGURE 5

(A) Representation of the microbiota in different tissues of A. vulgare (modified from Dittmer et al., 2016). Note that data from males and females are combined, therefore the chart illustrating the microbiota in the gonads represents both male and female gonads. The legend for all charts is the same as in (C). (B,C) The microbiome of A. vulgare for all tissues combined, at the phylum (B) and genus (C) level. Proteobacteria are represented at class level. Legends show the 15 most abundant phyla/classes and genera, respectively.