Deep-sea hydrothermal plumes have been considered natural laboratories for understanding the ecology, physiology, and function of microbial groups. Previous studies focused on interactions between microorganisms and inorganic, reduced hydrothermal inputs including sulfur, hydrogen, iron, and manganese. However, little is known about transformations of organic compounds, especially methylated, sulfur-containing compounds, and petroleum hydrocarbons. Gammaproteobacterial groups, like Methylophaga, Cycloclasticus, and Methanococcales, have been found to be dominant/prevalent in Deepwater Horizon oil spill or marine methane/oil seeps. Furthermore, Cycloclasticus has been discovered to be an obligate oil-degrading genus. Considering the similar hydrocarbon-rich settings in oil spill and hydrothermal plumes, we came up with a hypothesis that they can also live and thrive in hydrothermal plume.

Due to lack of omics-based metabolism references, we investigated all the plume metagenomes from plume samples (Guaymas Basin, Mid-Cayman Rise, and Lau Basin) to search these three gammaproteobacterial groups. We reconstructed nine gammaproteobacterial metagenome-assembled genomes (MAGs), and also mapped corresponding metatranscriptomic reads to enable genome-specific measurements and quantitative analyses of metabolic activities. We reconstructed detailed pathways for the metabolism of five groups of substrates (methylated and C₁ compounds, sulfur-containing organics, PAHs, methane and alkanes, and sulfur cycling-related compounds) that had been understudied heretofore. Metabolic functions have been illustrated in Fig. 1b. Furthermore, Metatranscriptomic evidence showed these three groups have high transcriptional activities of genes encoding cycling of C₁-compounds, petroleum hydrocarbons, and organic sulfur.

The oxidation of methanethiol (MT), the simplest thermochemically-derived organic sulfur, for energy metabolism in Methanococcales and Cycloclasticus was evidenced by omics-based inference and also supported with the existence of MT-bond as revealed by spectroscopic data of the particulate sulfur pool. Furthermore, low temperature mixed fluids in Guaymas Basin and Cayman plumes are enriched in MTs (up to 10³–10⁴ nM), which is consistent with the high expression level of MT oxidation operon.

The first near-complete MAG of hydrothermal Methylophaga aminisulfidivorans and its transcriptional profile point to active chemotaxis targeting small organic compounds. These Gammaproteobacteria are prevalent in global marine water columns and have methyl-accepting chemotaxis mechanisms for searching preferable eco-niches with substantial substrates (for Cycloclasticus and Methylophaga). Petroleum hydrocarbon-degrading Cycloclasticus are abundant and active in plumes of oil spills as well as deep-sea vents, suggesting that they are indigenous and effectively respond to stimulus of hydrocarbons in the deep sea (Fig. 1a).

Additionally, the heterotrophic degradation of marine dissolved organic matter (DOM) stimulates the activity of methylotrophs (e.g., Methylophaga), potentially through degradation of DOM methyl sugars to the substrates of methylotrophs such as methanol or formaldehyde. Marine DOM is universally distributed in the ocean. Thus, this successive and synergistic incorporation of DOM could in part explain the ubiquitous distribution of marine methylotrophs in the open ocean.

These findings suggest that these three groups of Gammaproteobacteria transform organic carbon and sulfur compounds via versatile and opportunistic metabolism and modulate biogeochemistry in plumes of hydrothermal systems as well as oil spills, thus contributing broad ecological impact to the deep ocean globally.

Link for the original publication:https://www.nature.com/articles/s41396-020-00745-5