Dancing for Food in the Deep Sea: Bacterial Farming by a New Species of Yeti Crab

Abstract

Vent and seep animals harness chemosynthetic energy to thrive far from the sun's energy. While symbiont-derived energy fuels many taxa, vent crustaceans have remained an enigma; these shrimps, crabs, and barnacles possess a phylogenetically distinct group of chemosynthetic bacterial epibionts, yet the role of these bacteria has remained unclear. We test whether a new species of Yeti crab, which we describe as Kiwa puravida n. sp, farms the epibiotic bacteria that it grows on its chelipeds (claws), chelipeds that the crab waves in fluid escaping from a deep-sea methane seep. Lipid and isotope analyses provide evidence that epibiotic bacteria are the crab's main food source and K. puravida n. sp. has highly-modified setae (hairs) on its 3rd maxilliped (a mouth appendage) which it uses to harvest these bacteria. The ε- and γ- proteobacteria that this methane-seep species farms are closely related to hydrothermal-vent decapod epibionts. We hypothesize that this species waves its arm in reducing fluid to increase the productivity of its epibionts by removing boundary layers which may otherwise limit carbon fixation. The discovery of this new species, only the second within a family described in 2005, stresses how much remains undiscovered on our continental margins.

Molecular evidence of digestion and absorption of epibiotic bacterial community by deep-sea crab Shinkaia crosnieri

“…Based on these observations, it has been hypothesized that S. crosnieri and K. puravida ingest their epibiotic microbial populations directly via this typical feeding behaviour, and digest them in their digestive organs (Watsuji et al, 2010;Thurber et al, 2011). In this study, we found setae fragments in almost every S. crosnieri intestine (Figure 1), which strongly suggests that the setae were ingested via the combing behaviour in S. crosnieri.…”

“…The deep-sea vent galatheid crabs, S. crosnieri and K. puravida, frequently exhibit a typical behaviour where they comb their setae, which are covered with dense epibionts, using the third maxillipeds and then bringing the maxillipeds to the mouths, although this behaviour has not been observed in R. exoculata (Watsuji et al, 2010;Thurber et al, 2011). Based on these observations, it has been hypothesized that S. crosnieri and K. puravida ingest their epibiotic microbial populations directly via this typical feeding behaviour, and digest them in their digestive organs (Watsuji et al, 2010;Thurber et al, 2011).…”

“…Given that the typical feeding-like behaviour has been observed frequently in these deep-sea vent galatheid crabs in their natural habitats and under rearing conditions, it was predicted that deep-sea vent galatheid crabs such as S. crosnieri and K. puravida ingest epibiotic microbial populations and utilize them as their primary diet (Watsuji et al, 2010;Thurber et al, 2011). However, the nutritional transfer from the epibionts to the host has not been directly shown and its mechanism remains unclear.…”

“…In addition, several species of deep-sea vent invertebrates harbour bacteria (epibionts) that colonize the surfaces of specialized tissues such as the dorsal setae of the polychaete Alvinella pompejana, the gill chambers of the shrimp Rimicaris exoculata and the setae of the galatheid crabs Shinkaia crosnieri, Kiwa hirsuta and K. puravida (Polz and Cavanaugh, 1995;Cary et al, 1997;Goffredi et al, 2008;Watsuji et al, 2010;Thurber et al, 2011). The epibiotic microbial communities associated with these hosts are believed to have chemolithoautotrophic and methanotrophic products that support their hosts nutritionally, as well as the endosymbionts themselves (Goffredi et al, 2008;Grzymski et al, 2008;Watsuji et al, 2010;Thurber et al, 2011;Ponsard et al, 2012). Radioisotope-labelled tracer experiments suggest that R. exoculata epibionts achieve chemolithoautotrophic production by oxidizing reduced sulphur compounds and ferrous iron (Ponsard et al, 2012).…”

Inorganic carbon fixation by chemosynthetic ectosymbionts and nutritional transfers to the hydrothermal vent host-shrimp Rimicaris exoculata

“…Among the Crustacea, chemosynthetic epibioses are reported in only a few hydrothermal decapods: the shrimp Rimicaris exoculata (Segonzac et al, 1993), the galatheid crabs Kiwa hirsuta (Macpherson et al, 2005;Goffredi et al, 2008), Kiwa puravida (Thurber et al, 2011), and Shinkaia crosnieri (Miyake et al, 2007), and two amphipods from littoral sediments (Gillan and Dubilier, 2004; and sulphide-rich caves (Dattagupta et al, 2009). Most of these associations are regarded as nutritional ectosymbioses, but to date, there is little direct evidence of bacterial autotrophy and no direct demonstration of mutualistic nutritional bacteriahost interactions.…”