Evidence for the microbial basis of a chemoautotrophic invertebrate community at a whale fall on the deep seafloor: bone-colonizing bacteria and invertebrate endosymbionts

Abstract

To explore the microbial basis for a remarkable macrofaunal community at the site of a whale skeleton on the seafloor of the Santa Catalina Basin, we obtained samples of whale bone, bone-colonizing invertebrates, microbial mats, and the dominant fauna in the adjacent sulfide-rich sediments during Alvin expeditions in 1988 and 1991. Invertebrate tissues were examined by transmission electron microscopy (TEM) and mats and bone-penetrating bacteria by epifluorescence microscopy (EM). Tissues from the dominant bivalve Vesicomya c.f. gigas, the mytilid mussel Idasola washingtonia, and selected gastropods and limpets were also assayed chemically for enzymes diagnostic of sulfur- and methane-based chemoautotrophy and for stable carbon isotopic composition. Results of all analyses were consistent with dominant sulfur-based endosymbioses in the clam and mussel (the first record of endosymbiosis in the genus Idasola) and the general absence of methane symbioses at the site, strengthening the analogy of the whale-skeleton faunal community to those known from distant Pacific hydrothermal vent sites. Examples of minor endosymbionts, either nitrifying or methanotrophic cells according to internal membrane structures by TEM, raised the possibility of a supplemental mode of nutrition to the clam, or means to remove ammonia in the gill tissue, in the event of significant changes in the chemical environment.