Resistance to freezing conditions of endemic Antarctic polychaetes is enhanced by cryoprotective proteins produced by their microbiome

Author:

Buschi Emanuela12ORCID,Dell’Anno Antonio2,Tangherlini Michael3ORCID,Candela Marco45ORCID,Rampelli Simone45ORCID,Turroni Silvia4ORCID,Palladino Giorgia45ORCID,Esposito Erika67ORCID,Martire Marco Lo2ORCID,Musco Luigi8ORCID,Stefanni Sergio9ORCID,Munari Cristina10ORCID,Fiori Jessica67,Danovaro Roberto2ORCID,Corinaldesi Cinzia11ORCID

Affiliation:

1. Department of Ecosustainable Marine Biotechnology, Stazione Zoologica “Anton Dohrn,” Fano Marine Centre, Fano, Italy.

2. Department of Life and Environmental Sciences, Polytechnic University of Marche, Ancona, Italy.

3. Department of Research Infrastructures for Marine Biological Resources, Stazione Zoologica “Anton Dohrn,” Fano Marine Centre, Fano, Italy.

4. Department of Pharmacy and Biotechnology, University of Bologna, Bologna, Italy.

5. Fano Marine Center, the Inter-Institute Center for Research on Marine Biodiversity, Resources and Biotechnologies, Fano, Italy.

6. Department of Chemistry “G. Ciamician” Alma Mater Studiorum, University of Bologna, Bologna, Italy.

7. IRCCS Istituto delle Scienze Neurologiche di Bologna, Bologna, Italia.

8. Department of Biological and Environmental Sciences and Technologies, University of Salento, Lecce, Italy.

9. Department of Biology and Evolution of Marine Organisms, Stazione Zoologica “Anton Dohrn,” Villa Comunale, Napoli, Italy.

10. Department of Chemical and Pharmaceutical Sciences, University of Ferrara, Ferrara, Italy.

11. Department of Materials, Environmental Sciences and Urban Planning, Polytechnic University of Marche, Ancona, Italy.

Abstract

The microbiome plays a key role in the health of all metazoans. Whether and how the microbiome favors the adaptation processes of organisms to extreme conditions, such as those of Antarctica, which are incompatible with most metazoans, is still unknown. We investigated the microbiome of three endemic and widespread species of Antarctic polychaetes: Leitoscoloplos geminus , Aphelochaeta palmeri , and Aglaophamus trissophyllus . We report here that these invertebrates contain a stable bacterial core dominated by Meiothermus and Anoxybacillus , equipped with a versatile genetic makeup and a unique portfolio of proteins useful for coping with extremely cold conditions as revealed by pangenomic and metaproteomic analyses. The close phylosymbiosis between Meiothermus and Anoxybacillus and these Antarctic polychaetes indicates a connection with their hosts that started in the past to support holobiont adaptation to the Antarctic Ocean. The wide suite of bacterial cryoprotective proteins found in Antarctic polychaetes may be useful for the development of nature-based biotechnological applications.

Publisher

American Association for the Advancement of Science (AAAS)

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