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

Abstract

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.

Tree age affects carbon sequestration potential via altering soil bacterial community composition and function

“…Chloroflexi has a pathway for complete hydrolysis or oxidative degradation of a wide range of recalcitrant organic substances, and the 3-hydroxypropionate bicycle is an essential pathway for autotrophic and carbon fixation ( Shih et al, 2017 ). PICRUst gene function prediction showed a high abundance of functional genes involved in carbon degradation of difficult-to-catabolize carbons, such as lignin and cellulose, which is consistent with the “feast or famine” metabolic strategy that Chloroflexi may follow ( Liu et al, 2022 ). In addition, the abundance of functional genes during carbon fixation ( Figure 8B ) showed that korA, which is involved in the 3-hydroxypropionate bicycle, had the highest abundance, which was consistent with the CO 2 fixation and autotrophic mode of Chloroflexi.…”

Spatial variation and metabolic diversity of microbial communities in the surface sediments of the Mariana Trench

“…Because composition and capabilities of heterotrophic microbial communities play a critical role in the detrital carbon cycle in sediments ( Teske et al, 2011 ). Chloroflexi has potential to degrade a wide range of organic carbon, even harbored pathways for the complete hydrolytic or oxidative degradation of various recalcitrant organic matters ( Liu et al, 2022 ). α-Proteobacteria could utilize a variety of organic compounds, mainly including amino acids, nucleic acids, fatty acids and other low molecular weight compounds, as well as organic and aromatic hydrocarbons produced by algae ( Buchan et al, 2014 ; Mishamandani et al, 2016 ).…”