Microbial insights from Antarctic and Mediterranean shallow-water bone-eating worms

Abstract

Bone-eating worms of the genus Osedax (Annelida, Siboglinidae) form unique holobionts (functional entity comprising host and associated microbiota), highly adapted to inhabit bone tissue of marine vertebrates. These gutless worms have developed nutritional symbioses housing intracellular, horizontally acquired, heterotrophic bacteria hypothesised to harness nutrients from organic compounds, sequestered within the bone. Despite previous efforts, critical mechanisms mediating activity and acquisition of diverse bacterial assemblages remain unclear. Using 16S rRNA amplicon sequencing, we performed detailed taxonomic and predicted functional analyses shedding light on the microbial communities of two shallow-water Osedax species (Osedax deceptionensis and Osedax ‘mediterranea’) from contrasting habitats (Antarctic and Mediterranean Sea), in two tissue types (roots and palps). Comparative assessments between host species revealed distinct microbial assemblages whilst, within host species and body tissue, relative symbiont frequencies retained high variability. We reported relatively high abundances of microbes previously classified as primary endosymbionts, Ribotype 1 (order Oceanospirillales), and diverse likely secondary epibionts warranting further exploration as recurrent Osedax associates. Surprisingly, O. ‘mediterranea’ exhibited relatively low abundance of Oceanospirillales, but increased abundance of other potentially hydrocarbon degrading bacteria from the family Alteromonadaceae. We hypothesise the presence of functionally similar, non-Oceanospirillales primary endosymbionts within O. ‘mediterranea’. Functional metagenomic profiling (using 16S rRNA sequences) predicted broad metabolic capabilities, encompassing relatively large abundances of genes associated with amino acid metabolism. Comparative analyses between host body tissue communities highlighted several genes potentially providing critical functions to the Osedax host or that confer adaptations for intracellular life, housed within bone embedded host root tissues.

Deciphering a Marine Bone-Degrading Microbiome Reveals a Complex Community Effort

“…Metagenomic assembly, binning, taxonomic identification, ORF prediction, and annotation. For each sample type (Osedax mucofloris and bone surface biofilm communities), the quality-filtered metagenomic reads (Trimmomatic version 0.36) were coassembled with SPAdes v3.12 (94) for kmers 21,33,55,77, and 99, with the metaSPAdes-assembler option enabled (see Table S1 in the supplemental material for read counts). Binning was conducted on the resulting assemblies using the MetaWRAP pipeline (version 1.0.1) (95).…”

“…To date, only a few studies have been published that focus on microbial communities to understand the necessary complex interactions in bone degradation, mainly relying on 16S rRNA gene sequencing data (30)(31)(32)(33) and one metagenomic study of a whale fall (34). We here provide a first comprehensive overview and identify putative key functions involved in bone degradation of the marine bone microbiome retrieved from deployed bone material, including microbial communities from the gutless worm Osedax mucofloris and free-living microbial assemblages developing on the bone surface.…”

Quantifying dominant bacterial genera detected in metagenomic data from fish eggs and larvae using genus‐specific primers

“…Polaribacter species have been isolated from Antarctic soil and in biofilms on stones from the North Sea (Choo et al, 2020 ; Kim et al, 2013 ), and the genus was detected in the intestine of marine organisms and algae (Hyun et al, 2014 ; Nedashkovskaya et al, 2013 ; Wei et al, 2018 ). Alkalimarinus sediminis was isolated from marine sediment in Shandong Province, China (Zhao et al, 2015 ), and Alkalimarinus species were found in bone‐eating worms ( Osedax mediterranea ) from the Mediterranean Sea (Hewitt et al, 2020 ). Healthy and diseased Dentex and Sparus aurata (bony fishes) cultured in Spanish Mediterranean aquaculture contained Enterovibrio coralii strains and possibly Enterovibrio nigricans (Pascual et al, 2009 ).…”

The bone-degrading enzyme machinery: From multi-component understanding to the treatment of residues from the meat industry

“…Two relevant such sources are the microbial biofilms that develop on the surface of bones from shallow and deep water marine environments, and the symbionts of bone-dwelling worms, e.g., Osedax mucofloris . These bio-resources have been shown to have a wide microbial diversity, whose compositions and involvement in the various and successive events involved in the degradation of mature bone, have been investigated to some detail [14] , [15] , [16] , [17] , [18] , [19] , [20] , [21] , [22] , [23] , [24] , [25] , [26] , [27] . In this process, recent metagenome sequence analyses suggested that, as mentioned above, the acidification by some organisms is key before the hydrolysis of bone matrix is initiated by other community members [27] .…”