Novel Chloroflexi genomes from the deepest ocean reveal metabolic strategies for the adaptation to deep-sea habitats

Abstract

\n Background: The deep-sea harbors the majority of the microbial biomass on Earth, and is a key site for organic matter (OM) remineralization and storage in the biosphere. Microbial metabolisms in the deep ocean are greatly controlled by the generally depleted but periodically fluctuating supply of OM. Currently, little is known about metabolic potentials of dominant deep-sea microbes to cope with the variable OM inputs, especially for those living in the hadal trenches - the deepest part of the ocean. Results: In this study, we report the first extensive examination of the metabolic potentials of hadal sediment Chloroflexi, a dominant phylum in hadal trenches and the global deep ocean. Sixty-two metagenome-assembled-genomes (MAGs) were reconstructed from nine metagenomic datasets derived from sediments of the Mariana Trench. These MAGs represent six novel species, four novel genera, one novel family and one novel order within the classes Anaerolinea and Dehalococcoidia. Fragment recruitment showed that these MAGs are globally distributed in deep-sea waters and surface sediments, and transcriptomic analysis indicated their in-situ activities. Metabolic reconstruction showed that hadal Chloroflexi mainly have a heterotrophic lifestyle, with the potential to degrade a wide range of organic carbon, sulfur and halogenated compounds. Our results reveal for the first time that hadal Chloroflexi harbor pathways for the complete hydrolytic or oxidative degradation of various recalcitrant OM, including aromatic compounds (e.g. benzoate), polyaromatic hydrocarbons (e.g. fluorene), polychlorobiphenyl (e.g. 4-chlorobiphenyl) and organochlorine compounds (e.g. chloroalkanes, chlorocyclohexane). Moreover, these organisms show the potential to synthesize energy storage compounds (e.g. trehalose), and have regulatory modules to respond to changes in nutrient conditions. These metabolic traits lead us to postulate that the Chloroflexi may follow a “feast and famine” metabolic strategy, which allows them to efficiently consume labile OM and store the energy under rich OM conditions, and to survive under OM limitations by utilizing stored energy and degrading recalcitrant OM. Conclusion: This study expands the knowledge on metabolic processes in deep-ocean Chlorolfexi, and highlights their significance in deep-sea carbon, sulfur and halogen cycles. The metabolic plasticity likely provides Chloroflexi with advantages for the survival under variable and heterogenic OM inputs in the deep ocean.