Microbiome reconstruction of in situ incubations reveals key players in polymer degradation in Arctic deep-sea hydrothermal sediments

Deep-sea hydrothermal vents are among the most extreme habitats on Earth and represent interesting targets for marine bioprospecting and biodiscovery. However, the full extent of the microbial heterotrophic capabilities at these environments is still being explored. Metagenomic studies already found that previously uncultured heterotrophic microorganisms control the carbon flow in hydrothermal deep-sea sediments through organic matter decomposition. Therefore, these habitats constitute important environments to find new microbial solutions that are urgently needed in the bioprocessing industry, where the degradation of complex organic materials is often a major challenge.

Here, we report on the development and the enrichment strategy of novel in situ incubators to investigate the degradation processes of the natural polymer chitin and artificial plastic polymers, like PET and HDPE. Sequence data of in situ enrichments with sediment samples from the Jan Mayen and the newly discovered Jøtul vent field show changes in the microbial community structure and indicate responsible microorganisms involved in the polymer degradation processes.

In addition to typical heterotrophic microorganisms, we identified potential novel chitin degraders within the uncultivated candidate phylum KSB1. These microorganisms are of particular interest, because they could neither be cultivated before, nor their role in carbon metabolism was described. By using different bioinformatical approaches we identified various chitin degrading enzymes of the KSB1 phylum. After heterologous expression and purification, the respective enzymes showed high chitin-degrading activity, demonstrating a significant role in the carbon cycle for KSB1 bacteria. The combined in situ incubation of chitin and plastic polymers also indicated an accelerated degradation of plastic polymers. By sequencing the transcriptomes, it was possible to reconstruct the microbiomes and uncover the underlying metabolic processes.

These results indicate that polymer degrading microorganisms were enriched in situ and play a critical role in the sediments carbon cycling. It is suggested that the mentioned microorganisms are important players in organic matter utilization/breakdown in deep-sea hydrothermal vents. Furthermore, the identified novel lineages are likely adapted to dealing with the industrial substrates in the incubation chambers, and thus provide novel sources for enzyme mining.