Coupled Carbon, Sulfur, and Nitrogen Cycles Mediated by Microorganisms in the Water Column of a Shallow-Water Hydrothermal Ecosystem

Abstract

Shallow-water hydrothermal vent ecosystems are distinctly different from deep-sea vents, as other than geothermal, sunlight is one of their primary sources of energy, so their resulting microbial communities differ to some extent. Yet compared with deep-sea systems, less is known about the active microbial community in shallow-water ecosystems. Thus, we studied the community compositions, their metabolic pathways, and possible coupling of microbially driven biogeochemical cycles in a shallow-water hydrothermal vent system off Kueishantao Islet, Taiwan, using high-throughput 16S rRNA sequences and metatranscriptome analyses. Gammaproteobacteria and Epsilonbacteraeota were the major active bacterial groups in the 16S rRNA libraries and the metatranscriptomes, and involved in the carbon, sulfur, and nitrogen metabolic pathways. As core players, Thiomicrospira, Thiomicrorhabdus, Thiothrix, Sulfurovum, and Arcobacter derived energy from the oxidation of reduced sulfur compounds and fixed dissolved inorganic carbon (DIC) by the Calvin-Benson-Bassham (CBB) or reverse tricarboxylic acid cycles. Sox-dependent and reverse sulfate reduction were the main pathways of energy generation, and probably coupled to denitrification by providing electrons to nitrate and nitrite. Sulfur-reducing Nautiliaceae members, accounting for a small proportion in the community, obtained energy by the oxidation of hydrogen, which also supplies metabolic energy for some sulfur-oxidizing bacteria. In addition, ammonia and nitrite oxidation is another type of energy generation in this hydrothermal system, with marker gene sequences belonging to Thaumarchaeota/Crenarchaeota and Nitrospina, respectively, and ammonia and nitrite oxidation was likely coupled to denitrification by providing substrate for nitrate and nitrite reduction to nitric oxide. Moreover, unlike the deep-sea systems, cyanobacteria may also actively participate in major metabolic pathways. This study helps us to better understand biogeochemical processes mediated by microorganisms and possible coupling of the carbon, sulfur, and nitrogen cycles in these unique ecosystems.

Geomicrobiology of a seawater-influenced active sulfuric acid cave

“…Members of these genera are typically associated with marine and halophilic water habitats, featured by chemolithotrophic activities related to sulfur and sulfidic compounds oxidation, and nitrogen metabolism in anoxia and absence of light [57–60]. In association with chemolithotrophs, FC filaments host marine oligotrophic Gammaproteobacteria Cellvibrionales and Alteromonadales members, the latter being considered dominant colonizers of marine biofilms able to metabolize various hydrocarbon compounds [61], which are also possibly involved in nitrogen and sulfur metabolism in shallow-water hydrothermal vent ecosystems [62].…”

Synechococcus sp. Strain PCC7002 Uses Sulfide:Quinone Oxidoreductase To Detoxify Exogenous Sulfide and To Convert Endogenous Sulfide to Cellular Sulfane Sulfur

“…In some habitats, they will encounter sulfide. The sulfur cycle is generally coupled with the carbon cycle (46)(47)(48); however, it is still unclear how sulfide affects Synechococcus spp. and how they deal with it.…”

Carbon Cycling in the World's Deepest Blue Hole

“…For example, the porosity of reef rocks is usually lower than 10% for limestone if the degree of fracturing is low (Manger, ), and thus, it is assumed that there is low water permeability of the deep rock of the YBH, as suggested by the ADCP results (Figure S1). In addition, hydrological, physical‐chemical, and biological properties of the deep YBH water column are not consistent with those of hydrothermal or cold seep environments (Peckmann & Thiel, ; Li, Tang, et al, ).…”