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

Olivia H Hewitt,Cristina Díez-Vives,Sergi Taboada

doi:10.1007/s00300-020-02731-1

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.

Highlights

Unique, specialist adaptations are critical for the survival of diverse organisms within nutrient limited, competitive marine zones
A total of 14 core amplicon sequence variants (ASVs) were present in all root samples from both species and 16 core ASVs were present in all root and palp samples from O. deceptionensis
We identified three core Oceanospirillales ASVs shared across all palp and root samples of O. deceptionensis (ASV960, ASV1445, ASV2484), but none shared between all root samples of O. deceptionensis and O. ‘mediterranea’ (Online Resource 2a)

Summary

Introduction

Specialist adaptations are critical for the survival of diverse organisms within nutrient limited, competitive marine zones. The death and fall of large marine mammals can bring temporary and successional oases within such environments, as macrofaunal communities compete to exploit these large influxes of organic matter (Smith and Baco 2003). One such specialist, Osedax (Annelida, Siboglinidae) (Goffredi et al 2004; Rouse et al 2004) have successfully colonised these unusual habitats, feeding and living within vertebrate bones from shallow and deep waters of the Pacific, Atlantic and Antarctic Oceans, and even the Mediterranean Sea (see Fujiwara et al 2019). We know of 26 Osedax species (Rouse et al 2004, 2008, 2015; Glover et al 2005, 2013; Fujikura et al 2006; Braby et al 2007; Fujiwara et al 2007; Goffredi et al 2007; Vrijenhoek et al 2008, 2009; Amon et al 2014; Taboada et al 2015; Sumida et al 2016), of which 15 were formally described within the last few years (Rouse et al 2018; Fujiwara et al 2019), and a few, as yet remain undescribed, demonstrating the increased knowledge of Osedax prevalence and diversity

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