Archaea and bacteria mediating anaerobic alkane degradation at its upper temperature limit

Abstract

Deep in the seafloor, geothermal heat transforms organic matter into alkanes and other petroleum compounds. These compounds migrate towards the sediment surface, where microorganisms consume them as carbon and energy source. In marine sediments, alkane degradation is predominantly coupled to sulfate reduction. This process is largely performed by archaea of the phylum Halobacteriota with methyl/alkyl-coenzyme M reductases (Mcr/Acr), which form syntrophic consortia with sulfate-reducing bacteria (SRB). Most of these organisms degrade alkanes shorter than pentane and at temperatures of maximum 60°C. In my thesis project, I cultured and characterized novel Mcr/Acr-encoding archaea and associated SRB from sediments of the Guaymas Basin (Gulf of California) beyond this temperature limit. Chapter 2 (Manuscript I) describes a novel consortium mediating anaerobic methane oxidation (AOM) at 70°C. The consortium consists of anaerobic methanotrophic archaea of the group ANME-1c and the thermophilic SRB Candidatus Thermodesulfobacterium torris. The ANME-1c is an ancestral ANME-1 clade that retains some characteristics of their thermophilic alkane-degrading relatives. The association of ANME-1c with Thermodesulfobacteria likely relies on direct interspecies electron transfer (DIET) via cytochromes. Chapter 3 (Manuscript II) describes the enrichment of Acr-encoding archaea of the phylum Hadarchaeota, which grow on the long-chain alkane hexadecane. Candidatus Cerberiarchaeum oleivorans and genomes from the same family encode the complete pathway for alkane degradation, which is not present in other Hadarchaeota. We propose that this Hadarchaeota family acquired some of the pathways for alkane degradation via horizontal gene transfer from other subsurface archaea. Chapter 4 (Manuscript III) shows that pathways related to DIET are widespread in Thermodesulfobacteria of marine environments. This suggests that other Thermodesulfobacteria species are potential syntrophic partners for anaerobic oxidation of alkanes. In Chapter 5, I discuss the findings of this thesis in the context of the evolution of archaea and alkane metabolisms. Acr-encoding archaea and associated SRB might occupy a broader variety of niches than previously thought. In summary, my thesis expands the occurrence of anaerobic methane and long-chain alkane metabolisms towards higher temperatures, now including archaea of the phylum Hadarchaeota.