Cultivation-Independent and Cultivation-Dependent Analysis of Microbes in the Shallow-Sea Hydrothermal System Off Kueishantao Island, Taiwan: Unmasking Heterotrophic Bacterial Diversity and Functional Capacity

Abstract

Shallow-sea hydrothermal systems experience continuous fluctuations of physicochemical conditions due to seawater influx which generates variable habitats, affecting the phylogenetic composition and metabolic potential of microbial communities. Until recently, studies of submarine hydrothermal communities have focused primarily on chemolithoautotrophic organisms, however, there have been limited studies on heterotrophic bacteria. Here, fluorescence in situ hybridization, high throughput 16S rRNA gene amplicon sequencing, and functional metagenomes were used to assess microbial communities from the shallow-sea hydrothermal system off Kueishantao Island, Taiwan. The results showed that the shallow-sea hydrothermal system harbored not only autotrophic bacteria but abundant heterotrophic bacteria. The potential for marker genes sulfur oxidation and carbon fixation were detected in the metagenome datasets, suggesting a role for sulfur and carbon cycling in the shallow-sea hydrothermal system. Furthermore, the presence of diverse genes that encode transporters, glycoside hydrolases, and peptidase indicates the genetic potential for heterotrophic utilization of organic substrates. A total of 408 cultivable heterotrophic bacteria were isolated, in which the taxonomic families typically associated with oligotrophy, copiotrophy, and phototrophy were frequently found. The cultivation-independent and -dependent analyses performed herein show that Alphaproteobacteria and Gammaproteobacteria represent the dominant heterotrophs in the investigated shallow-sea hydrothermal system. Genomic and physiological characterization of a novel strain P5 obtained in this study, belonging to the genus Rhodovulum within Alphaproteobacteria, provides an example of heterotrophic bacteria with major functional capacity presented in the metagenome datasets. Collectively, in addition to autotrophic bacteria, the shallow-sea hydrothermal system also harbors many heterotrophic bacteria with versatile genetic potential to adapt to the unique environmental conditions.

Nitrospina-Like Bacteria Are Potential Mercury Methylators in the Mesopelagic Zone in the East China Sea

“…For hgcB , the sequences without two strictly conserved CX 2 CX 2 CX 3 C motifs were removed ( Smith et al, 2015 ; Gionfriddo et al, 2016 ) after alignment using MEGA-X software. An effective estimation of hgcAB gene abundance from metagenomic sequences was normalized to the recA gene, which is an essential single-copy gene of bacteria ( Tang et al, 2018 ). The HMM reference for the recA gene was constructed using PF00154 representative protein sequences.…”

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

“…Most microbes in deep-sea hydrothermal vent ecosystems carry out chemosynthesis, which fixes carbon dioxide (CO 2 ) into organic compounds using the energy released by chemical reactions; it does not require sunlight. However, 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 ; Gomez-Saez et al, 2017 ; Tang et al, 2018 ). Previous surveys of bacterial 16S rRNA genes using tag pyrosequencing and clone libraries revealed a high abundance of chemoautotrophs within the classes Gammaproteobacteria and Epsilonproteobacteria (reclassified to a new phylum Epsilonbacteraeota; Waite et al, 2017 ) in shallow-water hydrothermal systems ( Tang et al, 2013 ; Gomez-Saez et al, 2017 ).…”

“…Thus, steep geochemical gradients form when reduced hydrothermal fluids meet the oxidized seawater. Electron donors in the gradients include sulfur (S 0 ), thiosulfate (S 2 O 3 2- ), hydrogen (H 2 ), organics, formate and fumarate, while nitrate, oxygen (O 2 ), S 0 , and S 2 O 3 2- are the major identified electron acceptors ( Xie et al, 2011 ; Anantharaman et al, 2016 ; Tang et al, 2018 ). Thus, a series of redox reactions occur and drive the carbon, nitrogen, and sulfur cycles in this hydrothermal ecosystem, which consists of the vent fluids and the water surrounding the vent.…”

Pseudopontixanthobacter vadosimaris gen. nov., sp. nov., isolated from shallow sea near Kueishan Island

“…This diversity of habitats suggests the wide distribution of the family members. Shallow-sea hydrothermal systems, with depths of less than 200 m below sea level and located along arcs, mid-ocean ridges and in island arc-related environments and even in continental margins have been shown to harbour communities with high physiological, metabolic and phylogenetical diversity [20]. In the present study, we describe the taxonomic characterization of a novel genus in the family Erythrobacteraceae , which was isolated from surface water of a shallow-sea hydrothermal system.…”