The phylogeography and ecology of Oligobrachia frenulate species suggest a generalist chemosynthesis-based fauna in the arctic

Heliyon · 7 authors, 8 centres

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TL;DR

Ancient DNA analysis revealed that museum specimen Oligobrachia webbi is genetically identical to the seep species O. haakonmosbiensis, and stable isotope data show Arctic chemosymbiotic frenulates occupy both seep and non-seep reducing habitats, indicating they are habitat generalists rather than seep specialists.

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The authors used ancient DNA (aDNA) methods to sequence museum voucher samples of the frenulate siboglinid polychaete Oligobrachia webbi and found 99% pairwise identity for 574 bp mtCOI fragments with O. haakonmosbiensis, resolving a long-standing taxonomic debate. Sediment geochemistry from fjords and sounds revealed reduced conditions with methane and sulfide buildup comparable to seep systems, sustained by terrestrial and marine organic matter decomposition. The authors suggest Arctic glacial history created widespread reducing environments, selecting for generalist chemosymbiotic species. Limitations include small sample sizes across sites and the inability to distinguish S. fiordicum from S. ekmani in frozen Nordfjord samples.

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biomedical research

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ORIGINAL PAPER

PMC10034460

The phylogeography and ecology of Oligobrachia frenulate species suggest a generalist chemosynthesis-based fauna in the arctic

Heliyon

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ABSTRACT

We used ancient DNA (aDNA) extraction methods to sequence museum voucher samples of Oligobrachia webbi, a frenulate siboglinid polychaete described from a northern Norwegian fjord over fifty years ago. Our sequencing results indicate a genetic match with the cryptic seep species, Oligobrachia haakonmosbiensis (99% pairwise identity for 574 bp mtCOI fragments) . Due to its similarity with O. webbi , the identity of O. haakonmosbiensis has been a matter of debate since its description, which we have now resolved. Furthermore, our results demonstrate that chemosynthesis-based siboglinids, that constitute the bulk of the biomass at Arctic seeps are not seep specialists. Our data on sediment geochemistry and carbon and nitrogen content reveal reduced conditions in fjords/sounds, similar to those at seep systems. Accumulation and decomposition of both terrestrial and marine organic matter results in the buildup of methane and sulfide that apparently can sustain chemosymbiotic fauna. The occurrence of fjords and by extension, highly reducing habitats, could have led to Arctic chemosymbiotic species being relatively generalist with their habitat, as opposed to being seep or vent specialists. Our stable isotope analyses indicate the incorporation of photosynthetically derived carbon in some individuals, which aligns with experiments conducted on frenulates before the discovery of chemosynthesis that demonstrated their ability to take up organic molecules from the surrounding sediment. Since reduced gases in non-seep environments are ultimately sourced from photosynthetic processes, we suggest that the extreme seasonality of the Arctic has resulted in Arctic chemosymbiotic animals seasonally changing their degree of reliance on chemosynthetic partners. Overall, the role of chemosynthesis in Arctic benthos and marine ecosystems and links to photosynthesis may be complex, and more extensive than currently known.

CITATION EXPORT

Arunima Sen, Liselotte W. Andersen, Kasper U. Kjeldsen et al.. The phylogeography and ecology of Oligobrachia frenulate species suggest a generalist chemosynthesis-based fauna in the arctic. Heliyon. (2023). https://doi.org/10.1016/j.heliyon.2023.e14232

AUTHORS

7 · 8 CENTRES

Arunima Sen, Liselotte W. Andersen, Kasper U. Kjeldsen, Loïc N. Michel, Wei Li Hong, Marvin Choquet, Tine L. Rasmussen

aDepartment of Arctic Biology, The University Centre in Svalbard (UNIS), Longyearbyen, Norway
bFaculty of Biosciences and Aquaculture, Nord University, Bodø, Norway
cDepartment of Biology, Section for Microbiology, Aarhus University, Aarhus, Denmark
dDepartment of Ecoscience, Aarhus University, Aarhus, Denmark
eUniv Brest, CNRS, Ifremer, UMR6197 BEEP (Biologie et Ecologie des Ecosystèmes Marins Profonds), Plouzané, France
fDepartment of Geological Sciences, Stockholm University, Stockholm, Sweden
gDepartment of Medical Biochemistry and Microbiology, Uppsala University, Uppsala, Sweden
hCentre for Arctic Gas Hydrate, Environment and Climate (CAGE), Department of Geosciences, The Arctic University of Norway, Tromsø, Norway