Abstract

The solar light response and photoelectrons produced by widespread semiconducting mineral play important roles in biogeochemical cycles on Earth’s surface. To explore the potential influence of photoelectrons generated by semiconducting mineral particles on nitrate-reducing microorganisms in the photic zone, a marine heterotrophic denitrifier Halomonas sp. strain 3727 was isolated from seawater in the photic zone of the Yellow Sea, China. This strain was classified as a Halomonadaceae. Whole-genome analysis indicated that this strain possessed genes encoding the nitrogen metabolism, i.e., narG, nasA, nirBD, norZ, nosB, and nxr, which sustained dissimilatory nitrate reduction, assimilatory nitrate reduction, and nitrite oxidation. This strain also possessed genes related to carbon, sulfur, and other metabolisms, hinting at its substantial metabolic flexibility. A series of microcosm experiments in a simulative photoelectron system was conducted, and the results suggested that this bacterial strain could use simulated photoelectrons with different energy for nitrate reduction. Nitrite, as an intermediate product, was accumulated during the nitrate reduction with limited ammonia residue. The nitrite and ammonia productions differed with or without different energy electron supplies. Nitrite was the main product accounting for 30.03% to 68.40% of the total nitrogen in photoelectron supplement systems, and ammonia accounted for 3.77% to 8.52%. However, in open-circuit systems, nitrite and ammonia proportions were 26.77% and 11.17%, respectively, and nitrogen loss in the liquid was not observed. This study reveals that photoelectrons can serve as electron donors for nitrogen transformation mediated by Halomonas sp. strain 3727, which reveals an underlying impact on the nitrogen biogeochemical cycle in the marine photic zone.

Highlights

  • Estuary and offshore ecosystems are transitional zones between freshwater/terrene systems and marine environments, which are affected by both terrestrial and anthropogenic transportations [1]

  • The effects of photoelectrons generated by semiconducting minerals in the marine photic zone on microorganisms are worth studying in the natural environment

  • Carbon Metabolism From the genomic information, strain 3727 is a putative chemoheterotrophic bacterium, as no genes involved in the carbon fixation pathway were found, but genes involved in some organic carbon metabolisms such as glycolysis, the tricarboxylic acid (TCA) cycle, the pentose phosphorylation pathway (PPP), and gluconeogenesis were identified (Table S1, Figure 3)

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Summary

Introduction

Estuary and offshore ecosystems are transitional zones between freshwater/terrene systems and marine environments, which are affected by both terrestrial and anthropogenic transportations [1]. The effects of photoelectrons generated by semiconducting minerals in the marine photic zone on microorganisms are worth studying in the natural environment. This study, aimed to explore the effects of photoelectrons generated by semiconducting mineral particles on prokaryote-mediated nitrate reduction in the photic zone of the estuary area of the Yellow Sea. To elucidate the influence mechanism, marine nitrate reducers were isolated from seawater in the photic zone of the Yellow Sea. Genomic sequencing and statistical analysis were employed to determine the phylogenetic status and metabolic potential of the isolation. The nitrate reduction pathways were verified with or without the influence of photoelectrons, which might help to clarify the influence of photoelectric effects of semiconducting minerals on the nitrogen metabolism of the isolate, which potentially shed light on the nitrogen biogeochemical cycle in the marine photic zone

Enrichment and Isolation of Nitrate Reducer
Nitrate and Nitrite Reduction Supplemented with Sodium Acetate
Photoelectron System Setup
Chemical Analysis Methods
Genome-Resolved Metagenomic and Phylogenetic Analyses
Draft Genome Features of Strain 3727
Carbon Metabolism
Nitrogen Metabolism
Sulfur Metabolism
Other Metabolisms
Conclusions
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