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

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.

Benthic Communities on the Mohn’s Treasure Mound: Implications for Management of Seabed Mining in the Arctic Mid-Ocean Ridge

“…In addition, it is already well established that hydrothermally active and non-active areas of the AMOR host unique and poorly studied macrofauna, as well as a wide diversity of novel and uncultured microbial biodiversity (e.g., Dahle et al, 2015Dahle et al, , 2018Steen et al, 2016;Stokke et al, 2020). Metagenomic studies from the AMOR have identified novel archaeal lineages, which have challenged our views on the origin and evolution of eukaryotes and the topology of the tree of life (Spang et al, 2015).…”

“…Metagenomic studies from the AMOR have identified novel archaeal lineages, which have challenged our views on the origin and evolution of eukaryotes and the topology of the tree of life (Spang et al, 2015). In addition, recent in situ enrichment and culture of rare sedimentary microbes at AMOR vents have revealed great potential for biodiscovery of novel enzymes for use in biorefining and bioconversion of industrially relevant substrates such as those produced in fish farming and wood-pulping industries (Stokke et al, 2020). Given the high degree of novel findings during work in the area over the most recent years, it is likely that they represent only the tip of the iceberg when it comes to the amount of potentially valuable genetic resources present in the AMOR region.…”

Microorganisms from deep-sea hydrothermal vents

“…Strains of the phylum Deferribacteres are the heterotrophic taxa commonly found in deep-sea vents that can grow with organic acids and proteinaceous compounds as energy sources, for example, Caldithrix abyssi (Miroshnichenko et al 2003b), Deferribacter abyssi (Miroshnichenko et al 2003a), D. autotrophicus (Slobodkina et al 2009a), D. desulfuricans (Takai et al 2003a, b, c). A high fraction of heterotrophic microbial lineages related to cultivated members within the order Thermotogales and Bacteroidetes, and many novel lineages were also enriched using a novel in situ enrichment strategy (Stokke et al 2020). Isolates in the phylum Deinococcus-Thermus have not only been isolated from hydrothermal vents but have often also been isolated from terrestrial hot springs.…”

“…The biopolymer lignin significantly stimulates the growth of the Bathyarchaeota subgroup Bathy-8 (Yu et al 2018). By deploying in situ enrichment carriers in hot marine hydrothermal sediments, some thermophilic heterotrophic microorganisms that have not yet been cultured have been identified (Stokke et al 2020). Enrichment cultures of electrotrophic communities are obtained on electrodes and show a specific enrichment of Archaea belonging to the Thermococcales and Archaeoglobales orders in microbial electrolysis cells (specially designed bio-electrochemical system) under hyperthermophilic conditions (80 °C) (Pillot et al 2018).…”

Exploring Codon Adjustment Strategies towards Escherichia coli-Based Production of Viral Proteins Encoded by HTH1, a Novel Prophage of the Marine Bacterium Hypnocyclicus thermotrophus

“…The discovery of the hydrothermal vent ecosystem remains one of the biggest breakthroughs in our understanding of how life can be sustained in extreme conditions, marked by the first vent observation on the Galápagos Rift, in the eastern Pacific [ 3 ] and the discovery of the first black smoker vents [ 4 ]. Today, hydrothermal vents are well-known as attractive sites for bioprospecting of biotechnologically interesting enzymes [ 5 , 6 , 7 , 8 ] and other valuable biomolecules with potential industrial applications [ 6 , 9 , 10 ]. As with other marine biomes [ 11 , 12 , 13 ], hydrothermal vent environments are observed to be abundant with viruses, especially tailed dsDNA bacteriophages of order Caudovirales [ 14 , 15 ].…”