Minireview Indigenous Ectosymbiotic Bacteria Associated with Diverse

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Minireview Indigenous Ectosymbiotic Bacteria Associated with Diverse Environmental Microbiology Reports (2010) doi:10.1111/j.1758-2229.2010.00136.x Minireview Indigenous ectosymbiotic bacteria associated with diverse hydrothermal vent invertebratesemi4_136 1..10 Shana K. Goffredi* Historical documentation suggests that the prevalence Biology Department, Occidental College, 1600 Campus and possible importance of these associations, whether Rd, Los Angeles, CA 90041, USA. beneficial or detrimental, was realized long ago (Ander- son and Stephens, 1969; Johnson et al., 1971; Sochard et al., 1979). Today, there are many well-known ectosym- Summary bioses involving hosts within at least three subgroups of Symbioses involving bacteria and invertebrates con- the Ciliophora, one Euglenozoan,twoNematoda subfami- tribute to the biological diversity and high productiv- lies, three Mollusca families, two classes of Annelida, and ity of both aquatic and terrestrial environments. many Crustacea, including both decapods and cirripeds Well-known examples from chemosynthetic deep-sea (Buck et al., 2000; Polz et al., 2000; Dubilier et al., 2008). hydrothermal vent environments involve ectosymbi- The vent shrimp Rimicaris exoculata, for example, pos- otic microbes associated with the external surfaces of sesses dense bacteria on its carapace and mouthparts marine invertebrates. Some of these ectosymbioses (Van Dover et al., 1988). Once thought to be a monocul- confer protection or defence from predators or the ture of a single, pleomorphic epsilonproteobacterium, it is environment itself, some are nutritional in nature, and now known that the bacterial community includes two many still are of unknown function. Several recently dominant bacterial types, whatever the prevailing chemi- discovered hydrothermal vent invertebrates, includ- cal conditions surrounding the animal (Gebruk et al., ing two populations of yeti crab (Kiwa spp.), a limpet 1993; Polz and Cavanaugh, 1995; Struck et al., 2008). (Symmetromphalus aff. hageni), and the scaly-foot Similarly, certain polychaetes (ex. Alvinella spp.), nema- snail (as yet undescribed), support a consortium of todes (ex. Laxus spp.), ciliates (ex. Zoothamnium diverse bacteria. Comparisons of these ectosymbio- niveum), and even amphipods (within the genus Niphar- ses to those previously described revealed similari- gus), to name a few, are colonized by one or a few, ties among the associated microorganisms, sometimes highly ordered bacterial phylotypes, whereas suggesting that certain microbes are indigenous to many other crustaceans, the nematode Eubostrichus, and the surfaces of marine invertebrates. In particular, certain molluscs, such as the peltospirid scaly-foot snail, members of the Thiovulgaceae (epsilonproteobacte- appear to associate with relatively diverse bacterial com- ria) and Thiotrichaceae (gammaproteobacteria) munities (Polz et al., 1994; 1999; Haddad et al., 1995; appear to preferentially form ectosymbioses with vent Goffredi et al., 2004; Rinke et al., 2006; Miyake et al., crustaceans and gastropods. Interactions between 2007; Goffredi et al., 2008; Dattagupta et al., 2009). specific Proteobacteria and the surfaces of many It has been suggested that ectosymbiosis is the first marine invertebrates likely have ecological and evo- step towards endosymbiosis and is the least intimate lutionary significance at these chemically challenging association on a large continuum from external attach- habitats. ment to extracellular to intracellular endosymbionts, with greater integration and coordination of host and symbiont towards the latter (Smith, 1979; Rosati, 2004). Certainly, Introduction evidence for this exists, including the phylogenetic simi- larity between the gammaproteobacterial ectosymbiont of Associations between bacteria and the body surfaces of Laxus spp. and the ‘Gamma 1’ endosymbiont of gutless aquatic invertebrates have been studied for decades. oligochaetes within the subfamily Phallodrilinae (Dubilier et al., 2008), as well as the sole gammaproteobacterial Received 4 October, 2009; accepted 14 December, 2009. *For cor- respondence. E-mail [email protected]; Tel. (+1) 323 259 1470; Fax ectosymbiont on the ciliate Z. niveum, which is most (+1) 323 341 4974. closely related to the endosymbiont of the scaly-foot snail © 2010 Society for Applied Microbiology and Blackwell Publishing Ltd 2 S. K. Goffredi (Rinke et al., 2006). However, evidence that ectobiota not source of nutrition (Van Dover et al., 1988; Ott et al., only exhibit, in many cases, some degree of site prefer- 1991; Polz et al., 1992; 1994; Bauer-Nebelsick et al., ence on the host (Goffredi et al., 2004) but also use spe- 1996; Rinke et al., 2006; Suzuki et al., 2009). Most crus- cific signalling between themselves and their host taceans exhibit grooming behaviour and for Rimicaris, in (Nussbaumer et al., 2004) suggests that surface associa- particular, ectosymbiont-like phylotypes have been tions are more than simply an incomplete step along the recovered from the gut, suggesting the very likely inges- path towards endosymbiotic integration. Arguably, these tion of these bacteria as a food source (Zbinden and ectosymbiotic associations, despite lesser morphological Cambon-Bonavita, 2003). In the case of the ciliate Ken- integration, can be complex and require significant trophoros, the food groove is dramatically reduced and molecular communication, recognition and coordination the ciliate is thought to rely exclusively on the phagocy- between partners, as is observed with the better-studied tosis of ectosymbionts for nutrition (Fenchel and Finlay, endosymbioses. 1989). It should be noted that this particular ectosym- Specific interactions between host and bacteria have bioses is also perpetuated via vertical transmission been observed for many ectosymbiotic associations, during binary fission between mother and daughter cells, including animal hosts that have soft tissue body sur- thus, too, suggesting a specific and stable association at faces, as in the case of alvinellid polychaetes, as well as time scales that go beyond the lifetime of an individual those that are covered in an exoskeleton or tough ‘non- host. living’ cuticle, such as members of the ecdysozoa (e.g. The external nature of invertebrate–microbe ectosym- nematodes and crustaceans). For example, in the bioses raises many interesting questions. For example, marine nematode Laxus oneistus, recognition and are there factors that predispose a particular bacterial binding by bacterial ectosymbionts are mediated by a group to a successful ectosymbiotic lifestyle? If so, can mannose-specific lectin secreted on the host cuticle patterns in the identity and distribution of these bacteria surface (Nussbaumer et al., 2004; Bulgheresi et al., be detected across diverse host species? Conversely, 2006). Even the rigid exoskeleton of crustaceans is con- does the host play a role in attracting the correct symbiont trolled, in part, by the activities of the host, and could and in maintaining the association, despite, in some thus exert control over the specific composition and dis- cases, periodic molting and lack of obvious special struc- tribution of microbes attaching to these surfaces. A tures for bacterial attachment? The purpose of this review recent report demonstrated that abundant filamentous was to add to a growing phylogenetic data set of ecto- bacteria on the exoskeleton of a cave amphipod (Niphar- symbiotic bacteria associated with hydrothermal vent gus sp.) were distinct from the free-living biofilm forming invertebrates, with primary emphasis on crustaceans and phylotypes found within the environment, suggesting a molluscs distributed broadly, with the intention of identify- highly specific association between these microbes and ing possible patterns that may help answer some of these their host (Dattagupta et al., 2009). In this particular outstanding questions. study, continuous reacquisition of the specific ectosym- biont by the amphipod, despite frequent molting and Hydrothermal vent ectosymbioses maintenance in aquaria for long periods, was observed (Dattagupta et al., 2009). Ectosymbiotic bacterial assemblages have been previ- The presumed reliance of many of these host animals ously described for a suite of taxonomically and geo- on their ectobiota suggests that evolutionary mecha- graphically diverse hydrothermal vent crustacean and nisms have ensured the recruitment and maintenance of gastropod hosts, including the originally described yeti a particular microbe or microbial community. For crab Kiwa hirsuta from the Pacific Antarctic Ridge and example, it is thought that the scaly-foot snail relies on another currently undescribed Kiwa species from Costa iron sulfide precipitation mediated by its deltaproteobac- Rica (Fig. 1A), a similarly hairy crab (Shinkaia crosnieri) terial ectobionts, which act to protect the snail from pre- from the Okinawa Trough, vent barnacles from both the dation (Goffredi et al., 2004). Similarly, it is widely known Lau Basin (undescribed sp. A) and Kermadec Arc, New that colonization of embryos and developing crustacean Zealand (Vulcanolepas osheai), the Mid-Atlantic Ridge larvae by specific bacteria affords protection against vent shrimp R. exoculata, and the ‘scaly-foot’ snail (cur- fungi and pathogenic bacteria, as well as from predators rently undescribed) from the Indian Ocean (Polz and (Gil-Turnes et al., 1989; Gil-Turnes and Fenical 1992; Cavanaugh, 1995; Southward and Newman, 1998; Gof- Lopanik et al., 2004). Additionally, aposymbiotic stilbone- fredi et al., 2004; 2008; Rinke et al.,
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