微生物学报

红树林紫泥弧菌ZWAL4003多元素代谢耦合过程实验解析

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李晨 ¹ , 王健鑫 ¹ , 夏梓钦 ¹ , 曾润颖 ² , 曲武 ¹

微生物学报 | Research Article 2026,66(6): 2898-2910

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微生物学报 | Research Article 2026, 66(6): 2898-2910

红树林紫泥弧菌ZWAL4003多元素代谢耦合过程实验解析

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李晨¹, 王健鑫¹, 夏梓钦¹, 曾润颖², 曲武¹

作者信息

^1.浙江海洋大学海洋科学与技术学院，浙江舟山

^2.自然资源部海洋生物资源开发技术创新中心，福建厦门

Experimental elucidation of multi-element metabolism coupling in the mangrove-derived Vibrio ziniensis ZWAL4003

Chen LI¹, Jianxin WANG¹, Ziqin XIA¹, Runying ZENG², Wu QU¹

Affiliations

^1.Marine Science and Technology College, Zhejiang Ocean University, Zhoushan, Zhejiang, China

^2.Technology Innovation Center for Exploitation of Marine Biological Resources, Ministry of Natural Resources, Xiamen, Fujian, China

出版时间: 2026-06-04 doi: 10.13343/j.cnki.wsxb.20250950

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摘要

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目的弧菌是驱动红树林沉积物中碳、氮、硫整体循环过程的重要参与者，但能够执行多种元素代谢过程的可培养弧菌菌株鲜有报道。本研究旨在验证红树林紫泥弧菌(Vibrio ziniensis) ZWAL4003参与碳、氮、硫等多元素代谢的功能，并揭示相关元素循环过程的互作关系及耦合机制。方法综合运用基因组分析、系统进化分析、16S rRNA基因丰度分析以及生理生化指标测定等方法探究ZWAL4003中潜在的元素代谢耦合过程。结果菌株ZWAL4003基因组中存在完整的三羧酸循环、氧化磷酸化、异化硝酸盐还原为铵及同化性硫还原相关基因。生理实验表明，葡萄糖、蔗糖、淀粉和甘油等碳源代谢可显著提升ZWAL4003的硝酸盐还原活性；而以NaNO₃作为氮源会抑制其硫酸盐还原活性，Na₂S₂O₃、Na₂SO₄和Na₂SO₃等硫源对硝酸盐还原活性存在抑制作用。此外，该菌株的16S rRNA基因近缘物种在我国东南沿海典型红树林沉积物中均有分布，相对丰度为0.004 19%-0.073 04%，且呈现出自北向南递增的趋势。结论本研究证实，在ZWAL4003菌株中碳源利用对硝酸盐和硫酸盐还原具有促进作用，而氮源和硫源的代谢活性存在相互抑制作用，进而形成了碳-氮-硫元素代谢的耦合过程。V. ziniensis在我国红树林生态系统中广泛分布，预示着该类群可能是该生态系统中元素循环耦合的重要执行者，本研究结果深化了对红树林生态系统微生物驱动的地球化学过程整体性的认知。

Abstract

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Objective Although the coupling of carbon (C), nitrogen (N), and sulfur (S) cycles is crucial in mangrove ecosystems, direct experimental evidence from pure microbial cultures demonstrating this coupling remains scarce. This work aims to elucidate the coupling process of C, N, and S cycles in mangrove-derived Vibrio ziniensis ZWAL4003. Methods An integrated approach combining genomic analysis, phylogenetic analysis, 16S rRNA gene abundance quantification, and physiological-biochemical characterization was employed to explore the potential coupling process of element metabolism in ZWAL4003. Results The genome of ZWAL4003 carried genes associated with complete metabolic pathways including tricarboxylic acid cycle, oxidative phosphorylation, dissimilatory nitrate reduction to ammonium, and assimilatory sulfur reduction. Glucose, sucrose, starch, and glycerol as C sources significantly enhanced the nitrate reduction activity of ZWAL4003. NaNO₃ as the N source inhibited the sulfate reduction activity of ZWAL4003. Na₂S₂O₃, Na₂SO₄, and Na₂SO₃ as the S sources inhibited the nitrate reduction activity. Furthermore, V. ziniensis strains were widely distributed in the mangrove sediments along the southeast coast of China, with the relative abundance of 0.004 19%-0.073 04%, showing an increasing trend from north to south. Conclusion This study demonstrates that C source utilization promotes nitrate and sulfate reductions, while mutual inhibition exists between nitrate and sulfate reductions, forming the coupling process of C, N, and S metabolisms in ZWAL4003. The wide distribution of V. ziniensis strains in the mangrove ecosystems of China suggests the potential important role of V. ziniensis as an executor in coupling element cycles. These findings enrich our understanding of the integrity of microbe-driven geochemical processes in mangrove ecosystems.

Key words

基因组学 / 红树林 / 弧菌 / 元素循环 / 耦合过程 / genomics / mangrove / Vibrio / element cycling / coupling process

引用本文

李晨, 王健鑫, 夏梓钦, 曾润颖, 曲武. 红树林紫泥弧菌ZWAL4003多元素代谢耦合过程实验解析. 微生物学报, 2026 , 66 (6) : 2898 -2910 . DOI: 10.13343/j.cnki.wsxb.20250950

Chen LI, Jianxin WANG, Ziqin XIA, Runying ZENG, Wu QU. Experimental elucidation of multi-element metabolism coupling in the mangrove-derived Vibrio ziniensis ZWAL4003[J]. Acta Microbiologica Sinica, 2026 , 66 (6) : 2898 -2910 . DOI: 10.13343/j.cnki.wsxb.20250950

正文

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Mangroves are rich in microbial resources that drive key processes in the chemical cycling of elements^[1]. The element cycle has proved to be a comprehensive process instead of an independent one in mangroves^[2]. About 30 chemical elements essential to life are coupled, thus the behavior of one element could be used to predict and manage that of other elements (e.g. carbon storage). However, the evidence of microbial pure culture that supports the multiple biogeochemical cycles and their coupling in mangrove sediments are unclear, which limits our knowledge of the ecological functions of this ecosystem.

The genus Vibrio represents a prevalent and ecologically significant group of microorganisms widely distributed in mangrove sediments^[3-4], water body^[5], and organisms^[6]. Owing to their rapid growth rates and high abundances, Vibrio actively participates in the cycling of C, N, and S, contributing substantially to the decomposition and turnover of organic matter^[7-8]. In our previous work, strain ZWAL4003 was isolated from mangrove sediments and identified as the type strain of a novel species, Vibrio ziniensis^[4]. Preliminary characterization revealed its involvement in complex biogeochemical processes, such as nitrate reduction and polysaccharide degradation^[4], suggesting that ZWAL4003 is an ideal model organism for investigating the coupling of multiple element metabolisms driven by Vibrio species.

We hypothesized that in V. ziniensis ZWAL4003: (1) The availability of labile carbon sources would stimulate both dissimilatory nitrate reduction and assimilatory sulfate reduction activities; (2) The presence of nitrate and sulfate/sulfite would mutually inhibit the reduction of the other, suggesting potential competition for intracellular reducing equivalents. We seek to provide a theoretical foundation for understanding the interactions and material cycling processes in mangrove sediments, ultimately contributing to the informed management and conservation of this ecosystem.

1 Materials and methods

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1.1 Genomic analysis of V. ziniensis ZWAL4003

The extraction of bacterial genomic DNA was carried out using the bacterial DNA Kit (Omega Bio-tek, USA), and the extraction operation was carried out according to the instructions. The genome was sequenced by using PacBio platform (Pacific Biosciences, USA) and was corrected by using the reads from Illumina HiSeq platform (Illumina, USA), which was completed by Shanghai Majorbio Bio-pharm Technology Co., Ltd. (China). The software of Unicycler v0.5.0 (https://github.com/rrwick/Unicycler) and SOAPdenovo2 (https://sourceforge.net/projects/soapdenovo2/) was used for genomic assembly, and Pilon v1.24 (https://github.com/broadinstitute/pilon/releases/tag/v1.24) was used for sequence correction. The coding sequences (CDSs) were predicted using Prodigal v2.6.3 (https://github.com/hyattpd/Prodigal). The metabolic pathway annotation was performed by using BLAST+ v2.3.0 (ftp://ftp.ncbi.nlm.nih.gov/blast/executables/blast+/2.3.0/) against KEGG database (http://www.genome.jp/kegg/). The sequences of tRNA and rRNA were predicted by using tRNAscan-SE v2.0 (http://trna.ucsc.edu/software/) and Barrnap v0.8 (https://github.com/tseemann/barrnap/), respectively. The analysis of gene islands, prophages, and CRISPR-Cas was completed by IslandPath-DIMOB v1.0.0 (http://www.pathogenomics.sfu.ca/islandviewer/), PHAST v1.0 (http://phast.wishartlab.com), and CRISPR Recognition Tool v1.0 (CRT, http://www.room220.com/crt), respectively. The genome plot was drawn by using Circos v0.69 (https://circos.ca/software/). The phylogenetic tree was constructed by using MEGA v6.0 (https://www.megasoftware.net/) with the neighbor-joining method and a bootstrap value of 1 000.

1.2 The determination of cell growth curve

V. ziniensis ZWAL4003 was inoculated into 50 mL 2216E medium containing 5 g/L peptone and 1 g/L yeast extract, then was cultured at 28 ℃ until OD₆₀₀ value reached 0.8 measured by using a microplate reader (Multiskan SkyHigh, ThermoFisher Scientific Inc., USA) at a wavelength of 600 nm. Subsequently, the culture was transferred into 50 mL fresh 2216E medium containing a mass fraction of 1% additional N (peptone, yeast extract, NH₄Cl, and NaNO₃) and S (Na₂S₂O₃, Na₂SO₄, and Na₂SO₃) sources. The volume fraction of inoculation was 1%. Mixture was cultured with a rotation speed of 200 r/min at 28 ℃ for 12 h. The broth sample was taken every 2 h, and the absorbance at 600 nm of the sample was determined to characterize the growth of bacterial strain. All experiments were performed with three biological replicates.

1.3 The determination of nitrate concentration

The bacterial cells were pre-cultured according to the method in section 1.2. The broth was transferred into 50 mL 2216E medium containing NaNO₃ with a mass fraction of 1%. Moreover, additional C (glucose, sucrose, starch, glycerol, CMC-Na, and citrate-Na) and S (Na₂S₂O₃, Na₂SO₄, and Na₂SO₃) sources at a final mass fraction of 1% were respectively supplemented in this medium. Then, the medium was cultured with a rotation speed of 200 r/min at 28 ℃ until OD₆₀₀ reached 0.8. The supernatant was sampled from the culture after centrifugation at 10 000 r/min, then NO₃^- content in supernatant was conducted by using the zinc-cadmium reduction method. Briefly, 25 mL sample was mixed with 0.5 mL CdCl₂ solution (20 g/L) and Zn sheets (99.99% purity), and then the mixture was shaken at 150 r/min for 10 minutes to reduce NO₃^- to NO₂^-. The absorbance at 543 nm was measured to calculate the concentration of NO₃^- based on the standard curve with a R² value of 0.999 4.

1.4 The measurement of sulfate concentration

The bacterial cells were pre-cultured according to the method in section 1.2. The broth was transferred into 50 mL 2216E medium containing Na₂SO₄ with a mass fraction of 1%. Moreover, additional C (glucose, sucrose, starch, glycerol, CMC-Na, and citrate-Na) and N (peptone, yeast extract, NH₄Cl, and NaNO₃) sources at a final mass fraction of 1% were respectively supplemented in this medium. Then, the medium was cultured with a rotation speed of 200 r/min at 28 ℃ until OD₆₀₀ reached 0.8. The supernatant was filtered through a 0.22 µm filter and SO₄^2- concentration was analyzed by using an ion chromatograph (ICS-2100, Multiskan SkyHigh, ThermoFisher Scientific Inc., USA) with the eluent of 8 mmol/L Na₂CO₃/1 mmol/L NaHCO₃ and a flow rate of 1.0 mL/min.

1.5 The calculation of 16S rRNA gene abundances of V. ziniensis strains from mangrove sediments in China

The mangroves along the southeast coast of China, including Fujian, Guangdong, and Guangxi Provinces, were selected. The clean sequencing data of 16S rRNA gene of the bacterial community in these mangrove sediments were downloaded from NODE (https://www.biosino.org/node/home) under the accession numbers of OEP001343, OEP001474, OEP001673, OEP001828, OEP001935 to OEP001948, and OEP002010. for calculating the relative abundance of V. ziniensis strains. The sequences with a similarity ≥97% to the 16S rRNA gene of ZWAL4003 were selected as the target sequences, and the relative abundance of V. ziniensis strain was calculated as the percentage of target sequence number to the total sequence number in the dataset.

1.6 Experimental design and statistical analysis

Three biological replicates were set for all biochemical assays in current study. Significant difference analysis was performed by using Student’s t-test in R software (version 4.5.2; https://www.r-project.org/).

2 Results and analysis

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2.1 Metabolic gene analysis of carbon, nitrogen, and sulfur sources in ZWAL4003 genomics

The complete genome of ZWAL4003 included two complete chromosomes with the lengths of 1 443 184 bp (G+C content 42.13%) and 3 207 372 bp (G+C content 43.12%), respectively (Figure 1). A total of 86.16% of sequences in ZWAL4003 genome was protein-coding, and 10, 10, and 11 genes in the genome encoded 16S, 23S, and 5S rRNA, respectively. Ten gene islands, 2 prophages, and 2 CRISPRs were annotated in ZWAL4003 genome. The key genes involved in C cycle, such as sugar metabolisms, tricarboxylic acid (TCA) cycle, and oxidative phosphorylation, were found in the genome sequences.

Furthermore, the complete pathways that participated in dissimilatory nitrate reduction to ammonium (DNRA; including 1 napA, 1 napB, 2 nirB, and 2 nirD genes) and assimilatory sulfur reduction (ASR; including 2 cysC, 2 cysD, 2 cysN, 1 cysH, 1 cysI, and cysJ) were annotated. These genes were phylogenetically closest to those with the accession numbers of WP 171138587.1 (Figure 2A), WP 416922594.1 (Figure 2B), WP 167410564.1 (Figure 2C), WP 171138556.1 (Figure 2D), WP 102941627.1 (Figure 2E), WP 171138557.1 (Figure 2F), WP 416921474.1 (Figure 2G), WP 202649566.1 (Figure 2H), WP 102966295.1 (Figure 2I), WP 275659734.1 (Figure 2J), WP 416923142.1 (Figure 2K),WP 416923140.1 (Figure 2L), WP 416921476.1 (Figure 2M), WP407834869.1 (Figure 2N), and WP 175579797.1 (Figure 2O) from Vibrio species.

2.2 The influences of carbon and sulfur sources on nitrate metabolism of V. ziniensis ZWAL4003

Glucose, sucrose, starch, and glycerol significantly increased the nitrate removal rate by 29.9%, 31.3%, 30.3%, and 14.6%, respectively (P<0.05). However, CMC-Na and citrate-Na decreased the nitrate removal rate by 47.9% and 88.3%, respectively (Figure 3A; P<0.05). The addition of sulfur sources of Na₂S₂O₃, Na₂SO₄, and Na₂SO₃significantly decreased the nitrate removal rate of V. ziniensis ZWAL4003, especially Na₂S₂O₃ and Na₂SO₃ completely inhibited the nitrate removal activity of this strain (Figure 3B; P<0.05). Therefore, glucose, sucrose, starch, and glycerol enhanced nitrate reduction activity of V. ziniensis ZWAL4003, whereas CMC-Na, citrate-Na, Na₂S₂O₃, Na₂SO₄, and Na₂SO₃ were inhibitory for this activity.

2.3 The influences of carbon and nitrogen sources on sulfate metabolism of V. ziniensis ZWAL4003

Glucose, sucrose, starch, and glycerol significantly increased the sulfate removal rate by 51.2%, 37.6%, 55.9%, and 27.0%, respectively (P<0.05). CMC-Na and citrate-Na significantly decreased the sulfate removal rate by 73.6% and 48.7%, respectively (Figure 3C; P<0.05). The nitrogen sources of peptone and NH₄Cl had no obvious influence on sulfate removal rate, while NaNO₃ significantly decreased the sulfate removal rate by 92.9% (Figure 3D; P<0.05). Therefore, peptone and NH₄Cl did not change the sulfate reduction activity of V. ziniensis ZWAL4003. Furthermore, glucose, sucrose, starch, and glycerol could improve the sulfate reduction activity of V. ziniensis ZWAL4003, while this activity was inhibited by CMC-Na, citrate-Na, and NaNO₃.

2.4 The influences of nitrogen and sulfur sources on cell growth of V. ziniensis ZWAL4003

Compared to the control group, the peptone promoted the cell growth of V. ziniensis ZWAL4003, whereas the yeast extract, NH₄Cl, and NaNO₃ delayed the growth of V. ziniensis ZWAL4003. Notably, the cell accumulation of V. ziniensis ZWAL4003 was lowest with the nitrogen source of NaNO₃ (Figure 3E). The additional sulfur sources of Na₂S₂O₃, Na₂SO₄, and Na₂SO₃ slowed down the cell growth of V. ziniensis ZWAL4003, and Na₂SO₃ mostly delayed the growth of V. ziniensis ZWAL4003 among these sulfur sources followed by Na₂S₂O₃ (Figure 3F).

2.5 The putative coupling process of carbon, nitrogen, and sulfur metabolisms in V. ziniensis ZWAL4003

Based on the above results, we inferred the interplay among the cell growth, nitrate and sulfate reductions as follows: (i) Most substrates for carbon utilization and oxidative phosphorylation enhanced the activities of nitrate and sulfate reductions; (ii) The substrates of nitrate and sulfate reductions exerted reciprocal inhibitory effects; (iii) The substrates of nitrate and sulfate reductions delayed cell growth. Based on biochemical data, the coupling process of carbon-nitrogen-sulfur metabolisms in V. ziniensis ZWAL4003 was supposed in Figure 4.

2.6 The distribution of V. ziniensis strains in mangrove sediments along the coast of China

Four locations with mangrove forests along the southeast coast of China, including Fujian, Guangdong, and Guangxi Provinces, were selected for calculating the relative abundance of 16S rRNA gene of V. ziniensis strains. The relative abundances of V. ziniensis strains were respectively 0.004 19%, 0.006 25%, 0.031 85%, and 0.073 04% in the mangrove sediments from these locations, and roughly increased from north to south in China (Figure 5).

3 Discussion

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Although the coupling of carbon, nitrogen, and sulfur cycles has been proposed in mangrove ecosystems based on metagenomic data, direct evidence from pure cultures that experimentally demonstrates such coupling remains limited^[9]. Previous studies have identified potential functional guilds—such as sulfur-driven denitrifiers or methane oxidizers coupled with sulfate reducers—through metagenome-assembled genomes (MAGs)^[2], but these findings rely on sequence assembly and inference, which may introduce uncertainties^[10]. In contrast, the present study provided experimental evidence from a pure culture of V. ziniensis ZWAL4003 to elucidate the coupling mechanisms among carbon, nitrogen, and sulfur metabolisms. By integrating genomic analysis with physiological assays, we offered an experimental basis for understanding multi-element metabolic coupling at the strain level.

This work demonstrated the existence of the coupling of carbon, nitrogen, and sulfur metabolisms in pure culture through biochemical experiments. This evidence avoids using the complex and error-prone algorithm for pathway analysis in metagenomic data. The results showed an actual promoting effect of carbon utilization on nitrate and sulfate reductions and a competition relationship between nitrate and sulfate reductions in V. ziniensis ZWAL4003, thereby providing a solid supporter for the biogeochemical cycle coupling in mangrove sediments. As a fast-growth genus^[8], Vibrio species greatly contributed to the material cycles in marine environments^[7], including mangrove sediments^[11]. Based on the biochemical measurement results, we suppose that the abundant storage of carbon sources and sulfate in mangrove sediments causes the strong positive coupling of carbon utilization and sulfate reduction and saves the limited nitrate in the sediments for potentially supporting the primary productivity of this ecosystem^[12] due to the competition between nitrate and sulfate reductions in V. ziniensis ZWAL4003.

The 16S rRNA gene of ZWAL4003, the type strain in V. ziniensis^[4], is phylogenetically clustered with those of V. plantisponsor MSSRF60 and V. diazotrophicus ATCC 33466, and these two strains possess the abilities of nitrogen fixation and nitrate reduction^[13-14], which suggests that this cluster positively involved in the nitrogen loss and supplement in sediments and soils. Furthermore, our findings revealed a wide distribution of V. ziniensis strains in the mangrove sediments along the southeast coast of China, indicating that the strains belonging to this species might be the potential important center that connected carbon, nitrogen, and sulfur cycles to form a holistic rather than an isolated element cycle system in mangroves from China. Nevertheless, we still need the relevant activities of the strain in the field environment in future research to determine its true ecological function in mangrove.

The coupling of carbon (C), nitrogen (N), and sulfur (S) cycles is likely driven by electron transfer derived from microbial oxidation of organic matter^[15-17]. Accordingly, we propose a putative coupling mechanism in V. ziniensis ZWAL4003: electrons generated from the oxidation of readily utilizable carbon sources (e.g., glucose) could be channeled to support the reductive steps of both dissimilatory nitrate reduction and assimilatory sulfate reduction, thereby enhancing these processes^[18-19], thereby enhancing the reduction activities. Conversely, the observed mutual inhibition between nitrate and sulfate reduction may stem from competition for intracellular reducing equivalents (electrons). Interestingly, CMC-Na and citrate-Na unexpectedly decreased the reduction activities for both nitrate and sulfate. We speculate that these specific carbon sources might redirect cellular reducing power towards alternative metabolic pathways, altering electron flow. These results point to complex, strain-specific metabolic networks and electron partitioning, underscoring the need for future studies employing metabolic flux and electron transfer analyses in V. ziniensis ZWAL4003.

4 Conclusion

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This study elucidates the genetic potential and physiological mechanism for the coupling of multiple element metabolisms in V. ziniensis ZWAL4003. Genomic analysis revealed complete pathways for oxidative phosphorylation, DNRA, and ASR. Physiological experiments provided compelling evidence that carbon source utilization promotes both nitrate and sulfate reductions, while a competitive interaction, likely for reducing equivalents, leads to mutual inhibition between the two pathways. The wide distribution of V. ziniensis strains in mangrove sediments along China’s coast suggests that this coupling mechanism is ecologically relevant, positioning this species as a potential player in multiple elemental cycles within this important ecosystem. This work provided evidence from a pure culture, widening our understanding of holistic, microbe-driven geochemical process in mangroves.

基金

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国家自然科学基金(42573055)
国家自然科学基金(42303064)
自然资源部海洋生物资源开发利用工程技术创新中心开放基金(TICMBR202406)

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2026年第66卷第6期

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文章信息

doi: 10.13343/j.cnki.wsxb.20250950

接收时间：2025-12-19
首发时间：2026-06-17
出版时间：2026-06-04

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文章信息

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出版历史

收稿日期：2025-12-19
录用日期：2026-03-11

基金

the National Natural Science Foundation of China(42573055)

国家自然科学基金(42573055)

the National Natural Science Foundation of China(42303064)

国家自然科学基金(42303064)

the Fund of the Technology Innovation Center for Exploitation of Marine Biological Resources, MNR(TICMBR202406)

自然资源部海洋生物资源开发利用工程技术创新中心开放基金(TICMBR202406)

作者信息

^1.浙江海洋大学海洋科学与技术学院，浙江舟山

^2.自然资源部海洋生物资源开发技术创新中心，福建厦门

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https://castjournals.cast.org.cn/joweb/wswxb/CN/10.13343/j.cnki.wsxb.20250950

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2种不同金属材料的力学参数

科 Family	属数 Number of genus	种数 Number of species	占总种数比例 Percentage of total species (%)	属 Genus	种数 Number of species	占总种数比例 Percentage of total species (%)
鹅膏菌科Amanitaceae	2	11	5.26	鹅膏菌属 Amanita	10	4.78
小菇科 Mycenaceae	2	12	5.74	丝盖伞属 Inocybe	5	2.39
多孔菌科 Polyporaceae	8	14	6.70	蜡蘑属 Laccaria	5	2.39
红菇科 Russulaceae	3	23	11.00	小皮伞属 Marasmius	6	2.87
				小菇属 Mycena	11	5.26
				光柄菇属 Pluteus	5	2.39
				红菇属 Russula	17	8.13
				栓菌属 Trametes	5	2.39

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