The Terrestrial Isopod Microbiome: an All-In-One Toolbox for Animal–Microbe Interactions of Ecological Relevance
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The Terrestrial Isopod Microbiome: An All-in-One Toolbox for Animal–Microbe Interactions of Ecological Relevance The Harvard community has made this article openly available. Please share how this access benefits you. Your story matters Citation Bouchon, Didier, Martin Zimmer, and Jessica Dittmer. 2016. “The Terrestrial Isopod Microbiome: An All-in-One Toolbox for Animal–Microbe Interactions of Ecological Relevance.” Frontiers in Microbiology 7 (1): 1472. doi:10.3389/fmicb.2016.01472. http:// dx.doi.org/10.3389/fmicb.2016.01472. Published Version doi:10.3389/fmicb.2016.01472 Citable link http://nrs.harvard.edu/urn-3:HUL.InstRepos:29408382 Terms of Use This article was downloaded from Harvard University’s DASH repository, and is made available under the terms and conditions applicable to Other Posted Material, as set forth at http:// nrs.harvard.edu/urn-3:HUL.InstRepos:dash.current.terms-of- use#LAA fmicb-07-01472 September 21, 2016 Time: 14:13 # 1 REVIEW published: 23 September 2016 doi: 10.3389/fmicb.2016.01472 The Terrestrial Isopod Microbiome: An All-in-One Toolbox for Animal–Microbe Interactions of Ecological Relevance Didier Bouchon1*, Martin Zimmer2 and Jessica Dittmer3 1 UMR CNRS 7267, Ecologie et Biologie des Interactions, Université de Poitiers, Poitiers, France, 2 Leibniz Center for Tropical Marine Ecology, Bremen, Germany, 3 Rowland Institute at Harvard, Harvard University, Cambridge, MA, USA 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 Edited by: represent keystone species in terrestrial ecosystems, contributing to the decomposition Ute Hentschel, GEOMAR – Helmholtz Centre for of organic matter and regulating the microbial food web. Since their nutrition is based Ocean Research Kiel, Germany on plant detritus, it has long been suspected that bacterial symbionts located in the Reviewed by: digestive tissues might play an important role in host nutrition via the provisioning Pepijn Wilhelmus Kooij, Royal Botanic Gardens, UK of digestive enzymes, thereby enabling the utilization of recalcitrant food compounds Yuval Gottlieb, (e.g., cellulose or lignins). If this were the case, then (i) the acquisition of these Hebrew University of Jerusalem, Israel bacteria might have been an important evolutionary prerequisite for the colonization Yongjie Wang Wang, Shanghai Ocean University, China of land by isopods, and (ii) these bacterial symbionts would directly mediate the role *Correspondence: of their hosts in ecosystem functioning. Several bacterial symbionts have indeed been Didier Bouchon discovered in the midgut caeca of terrestrial isopods and some of them might be specific [email protected] to this group of animals (i.e., Candidatus Hepatoplasma crinochetorum, Candidatus Specialty section: Hepatincola porcellionum, and Rhabdochlamydia porcellionis), while others are well- This article was submitted to known intracellular pathogens (Rickettsiella spp.) or reproductive parasites (Wolbachia Microbial Symbioses, a section of the journal sp.). Moreover, a recent investigation of the microbiota in Armadillidium vulgare has Frontiers in Microbiology revealed that this species harbors a highly diverse bacterial community which varies Received: 26 June 2016 between host populations, suggesting an important share of environmental microbes Accepted: 05 September 2016 in the host-associated microbiota. In this review, we synthesize our current knowledge Published: 23 September 2016 on the terrestrial isopod microbiome and identify future directions to (i) fully understand Citation: Bouchon D, Zimmer M and Dittmer J the functional roles of particular bacteria (both intracellular or intestinal symbionts and (2016) The Terrestrial Isopod environmental gut passengers), and (ii) whether and how the host-associated microbiota Microbiome: An All-in-One Toolbox for Animal–Microbe Interactions could influence the performance of terrestrial isopods as keystone species in soil of Ecological Relevance. ecosystems. Front. Microbiol. 7:1472. doi: 10.3389/fmicb.2016.01472 Keywords: bacterial diversity, endosymbionts, microbiota, symbiosis, ecological interactions, terrestrial isopods Frontiers in Microbiology | www.frontiersin.org 1 September 2016 | Volume 7 | Article 1472 fmicb-07-01472 September 21, 2016 Time: 14:13 # 2 Bouchon et al. The Terrestrial Isopod Microbiome INTRODUCTION When considering the wider microbial community beyond heritable endosymbionts, many insect microbiotas are of Over the last decade, research on animal–bacterial symbioses has relatively low diversity but highly specialized, such as in bees shifted from its historical focus on binary host–symbiont and flies (Koch and Schmid-Hempel, 2011; Martinson et al., interactions to a more holistic perspective, taking into 2011; Wong et al., 2011). At the other end of the spectrum account that symbioses are shaped by complex multipartite are the termites with their highly diverse hindgut community interactions between hosts and diverse symbiotic communities of bacteria, archaea, and protozoans involved in lignocellulose (the microbiome), partly acquired from the environment. This digestion (Hongoh, 2010; He et al., 2013; Peterson et al., 2015). “microbiome revolution” (Blaser, 2014) was mainly driven by the However, only very few studies have investigated microbiome advent of new high-throughput DNA sequencing technologies, patterns across ecologically diverse groups of insects, with the which enabled us to appreciate the diversity and ubiquity of exception of Colman et al. (2012). Their study demonstrated animal-associated microbiomes as an essential component of that microbiota composition was strongly influenced by host host biology as well as a source of evolutionary novelty (Ley diet in various insects. Specifically, bacterial diversity was highest et al., 2008; Fraune and Bosch, 2010; McFall-Ngai et al., 2013). in detritivorous and xylophagous species from different insect Hence, it is now established that the microbiome can modulate orders (termites and beetles) and their microbiotas were more host development (Shin et al., 2011), nutrition (Chandler et al., similar to each other compared to insects with other diets. 2011; He et al., 2013; Wong et al., 2014), immunity (Chu Overall, however, more studies in diverse non-model arthropods and Mazmanian, 2013), vector competence and susceptibility to across different ecological niches will be needed to complete pathogen infection (Dong et al., 2009; Koch and Schmid-Hempel, our understanding of host–microbiota interactions beyond the 2012), and speciation (Brucker and Bordenstein, 2012, 2013). insects. In this review, we present terrestrial isopod crustaceans as The majority of studies on arthropod microbiomes have been an emerging model organism to investigate arthropod–bacteria conducted in insects and have made enormous contributions to symbioses of evolutionary and ecological relevance. our understanding of intricate host–symbiont relationships. For instance, many insects feeding on nutrient-deficient diets such as plant sap or vertebrate blood maintain long-lasting associations TERRESTRIAL ISOPOD ECOLOGY AND with heritable obligate mutualistic endosymbionts (primary EVOLUTION symbionts) which provide essential nutrients (amino acids and vitamins) lacking from the host’s diet (Thao and Baumann, 2004; From an evolutionary perspective, oniscidean isopods are Moran et al., 2005; Pais et al., 2008; McCutcheon et al., 2009; the most successful colonizers of terrestrial habitats among McCutcheon and Moran, 2010). These symbionts are usually the Crustacea, comprising around 3700 species (Schmalfuss, harbored in specialized cells (the bacteriocytes), which may 2003). Originating from the marine littoral zone, they have form an additional host organ, the bacteriome. An even higher colonized almost all types of terrestrial environments on number of species harbor facultative intracellular symbionts Earth, including deserts, except for high alpine and polar (secondary symbionts). These are generally not required for regions (Figure 1). This makes them excellent model organisms host survival and reproduction, but may be beneficial under regarding evolutionary adaptations to a terrestrial lifestyle in certain environmental conditions, for instance through increased terms of reproduction, respiration, nutrition, excretion systems, thermal tolerance, host plant speciation, predator avoidance and protection against desiccation (reviewed in Hornung, 2011). and defense against natural enemies and parasites (Montllor The main morphological and physiological changes compared et al., 2002; Oliver et al., 2003, 2005; Ferrari et al., 2004; to marine crustaceans include (i) a reduction in body size, Tsuchida et al., 2004, 2010; Scarborough et al., 2005; Jaenike (ii) a water-resistant cuticle, (iii) pleopodal lungs, (iv) a water et al., 2010; Lukasik et al., 2013). Other facultative bacteria conducting system, and (v)