Association of Thioautotrophic Bacteria with Deep-Sea Sponges

Abstract

We investigated microorganisms associated with a deep-sea sponge, Characella sp. (Pachastrellidae) collected at a hydrothermal vent site (686 m depth) in the Sumisu Caldera, Ogasawara Island chain, Japan, and with two sponges, Pachastrella sp. (Pachastrellidae) and an unidentified Poecilosclerida sponge, collected at an oil seep (572 m depth) in the Gulf of Mexico, using polymerase chain reaction–denaturing gradient gel electrophoresis (PCR-DGGE) directed at bacterial 16S rRNA gene sequences. In the PCR-DGGE profiles, we detected a single clearly dominant band in each of the Characella sp. and the unidentified Poecilosclerida sponge. BLAST search of their sequences showed that they were most similar (>99% identity) to those of the gammaproteobacterial thioautotrophic symbionts of deep-sea bivalves from hydrothermal vents, Bathymodiolus spp. Phylogenetic analysis of the near-full length sequences of the 16S rRNA genes cloned from the unidentified Poecilosclerida sponge and Characella sp. confirmed that they were closely related to thioautotrophic symbionts. Although associations between sponges and methanotrophic bacteria have been reported previously, this is the first report of a possible stable association between sponges and thioautotrophic bacteria.Electronic supplementary materialThe online version of this article (doi:10.1007/s10126-009-9253-7) contains supplementary material, which is available to authorized users.

Evidence of a Putative Deep Sea Specific Microbiome in Marine Sponges

“…The other abundant group, thioautotrophic γ-Proteobacteria has previously been found within sponges [11], [37], and associated with other marine invertebrates such as marine tubeworms and shellfish [38]. This class of bacteria appears to be a frequent symbiont, present in many marine invertebrates.…”

“…A symbiotic relationship between marine tubeworms and sulphur oxidising bacteria is well established, with tubeworms dependent on nutrients supplied by sulphur oxidising chemoautotrophic γ-Proteobacteria [43]. A similar role for sulphur oxidising bacteria within sponges has not been shown although these bacteria appear to be widespread and abundant in deep sea sponges [37], [38]. There is also a report of a specific putative symbiosis between free-living marine Thaumarchaeota and sulphur-oxidising γ-Proteobacteria in sulphide rich mangrove swamps [44], implying that these two organisms themselves can form a close symbiotic relationship.…”

The Microbiome and Occurrence of Methanotrophy in Carnivorous Sponges

“…Sulfur- and ammonia-oxidizing symbionts seem to be common in non-carnivorous deep-sea sponges (Nishijima et al, 2010; Arellano et al, 2013), implying that chemolithoautotrophy could be a widespread supplementary source of nutrition for deep-sea sponges in general (Kennedy et al, 2014). Though the taxonomic affinity of the major putative sulfur-oxidizing groups in our dataset (Thiohalorhabdales, Oceanospirillales) were partly different than that of Kennedy et al (2014) (chiefly Chromatiales, but also some Oceanospirillales and others), this raises the possibility that partial nutrient acquisition from sulfur oxidation could be common in carnivorous sponges as well, though as evidenced by the isotope signatures from our study ( Figure 3 ) such activity would be a supplement to carnivory rather than the major mode of nutrition.…”

Clones or clans: the genetic structure of a deep‐sea sponge,Aphrocallistes vastus,in unique sponge reefs of British Columbia, Canada

“…Bacterial chemosynthesis at vent sites supports much of that life, and although associations of sponges with thioautotrophic bacteria may be more common than once thought (Nishijima et al . ), generally benthic suspension feeders such as sponges or corals tend to be associated with regions of downwelling (Pile & Young ), resuspension (Bett & Rice ) or enhanced flow such as is found over seamounts (Genin et al . ; Mehl et al .…”