Tailoring Hydrothermal Vent Biodiversity Toward Improved Biodiscovery Using a Novel in situ Enrichment Strategy.

Runar Stokke,Francesca Vulcano,Thomas Viflot,Rolf B Pedersen,Håkon Dahle,Ida H Steen,Solveig Lie Onstad,Eoghan P Reeves,Anita-Elin Fedøy,Vincent G H Eijsink

doi:10.3389/fmicb.2020.00249

Runar Stokke, Francesca Vulcano + Show 8 more

Open Access

https://doi.org/10.3389/fmicb.2020.00249

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Abstract

Deep-sea hydrothermal vents are amongst the most extreme environments on Earth and represent interesting targets for marine bioprospecting and biodiscovery. The microbial communities in hydrothermal vents are often dominated by chemolithoautotrophs utilizing simple chemical compounds, though the full extent of their heterotrophic abilities is still being explored. In the bioprocessing industry, where degradation of complex organic materials often is a major challenge, new microbial solutions are heavily needed. To meet these needs, we have developed novel in situ incubators and tested if deployment of recalcitrant materials from fish farming and wood-pulping industries introduced changes in the microbial community structure in hot marine hydrothermal sediments. The incubation chambers were deployed in sediments at the Bruse vent site located within the Jan Mayen vent field for 1 year, after which the microbial populations in the chambers were profiled by 16S rRNA Ion Torrent amplicon sequencing. A total of 921 operational taxonomic units (OTUs) were assigned into 74 different phyla where differences in community structure were observed depending on the incubated material, chamber depth below the sea floor and/or temperature. A high fraction of putative heterotrophic microbial lineages related to cultivated members within the Thermotogales were observed. However, considerable fractions of previously uncultivated and novel Thermotogales and Bacteroidetes were also identified. Moreover, several novel lineages (e.g., members within the DPANN superphylum, unidentified archaeal lineages, unclassified Thermoplasmatales and Candidatus division BRC-1 bacterium) of as-yet uncultivated thermophilic archaea and bacteria were identified. Overall, our data illustrate that amendment of hydrothermal vent communities by in situ incubation of biomass induces shifts in community structure toward increased fractions of heterotrophic microorganisms. The technologies utilized here could aid in subsequent metagenomics-based enzyme discovery for diverse industries.

Highlights

With the growing demands for utilization of enzymes in industrial, medical and biotechnological applications, the search for new and specialized enzymes is of fundamental importance
2www.arb-silva.de are lower than the two-phase boundary for seawater at the seafloor (271◦C), Cl contents lower than seawater indicate that the fluids have undergone phase separation, which may account for highly elevated CO2 and CH4 contents reported in Dahle et al (2018), and high CH4 reported here
Our study was designed to improve the potential for biodiscovery of novel enzymes for use in biorefining and bioconversion of industrially relevant substrates

Summary

Introduction

With the growing demands for utilization of enzymes in industrial, medical and biotechnological applications, the search for new and specialized enzymes is of fundamental importance. Metagenome-assembled genomes have further revealed that diverse, heterotrophic microorganisms, with unknown physiologies, control the carbon flow in marine and hydrothermal deep-sea sediments via organic matter decomposition (Lloyd et al, 2013; Dombrowski et al, 2017). Such microorganisms represent a great resource for finding new enzymes for biomedical, biotechnological, and industrial applications (Michalska et al, 2015). With the increasing demand for sustainable development based on the use of renewable raw materials, the importance of enzymes from hyperthermophiles in biomass conversions will likely increase

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