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

Yufang Li,Xiabing Xie,Yao Zhang,Chen-Tung Arthur Chen,Kai Tang,Deli Wang,Lianbao Zhang,Nianzhi Jiao,Zihao Zhao

doi:10.3389/fmicb.2018.02718

Yufang Li, Xiabing Xie + Show 7 more

Open Access

https://doi.org/10.3389/fmicb.2018.02718

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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.

Highlights

The discovery of marine hydrothermal vents greatly enhanced our understanding of microbial habitats and survival strategies as well as the origins of life
High-throughput 16S rRNA sequences and metatranscriptome analyses revealed that Gammaproteobacteria and Epsilonbacteraeota were the most active bacterial populations involved in the major carbon, sulfur, and nitrogen metabolic pathways in a shallow-water hydrothermal ecosystem
The major sulfur oxidizers were Thiomicrospira, Thiomicrorhabdus, and Thiothrix from Gammaproteobacteria, and Arcobacter and Sulfurovum from Epsilonbacteraeota, which showed high transcript abundances in the genes involved in the SOX/reverse sulfate reduction pathway

Summary

Introduction

The discovery of marine hydrothermal vents greatly enhanced our understanding of microbial habitats and survival strategies as well as the origins of life. Microbial communities in deep-sea hydrothermal systems have been intensively studied (Brazelton and Baross, 2010; Xie et al, 2011; Grosche et al, 2015; Anantharaman et al, 2016) since the discovery of these vents in 1977. Most microbes in deep-sea hydrothermal vent ecosystems carry out chemosynthesis, which fixes carbon dioxide (CO2) into organic compounds using the energy released by chemical reactions; it does not require sunlight. In shallow-water hydrothermal vent ecosystems, generally at water depths less than 200 m, chemolithoautotrophy and photoautotrophy occur simultaneously (Maugeri et al, 2009; Zhang et al, 2012; GomezSaez et al, 2017; Tang et al, 2018). Despite nearly 30 published studies on shallowwater hydrothermal systems, many open questions remain about the chemosynthetic and photosynthetic microbes, including the metabolic pathways they use, how the pathways are coupled with each other, and what factors control their ecology

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