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Article(id=1226855194030425055, tenantId=1146029695717560320, journalId=1192105938417971205, issueId=1226855188863038235, articleNumber=null, orderNo=null, doi=10.13343/j.cnki.wsxb.20250160, pmid=null, cstr=null, oa=null, hot=null, price=null, onlineType=0, articleFormat=0, articleType=null, articleTypeStr=research-article, receivedDate=1740672000000, receivedDateStr=2025-02-28, revisedDate=null, revisedDateStr=null, acceptedDate=1741881600000, acceptedDateStr=2025-03-14, onlineDate=1770434672124, onlineDateStr=2026-02-07, pubDate=1748966400000, pubDateStr=2025-06-04, doiRegisterDate=null, doiRegisterDateStr=null, onlineIssueDate=1770434672124, onlineIssueDateStr=2026-02-07, onlineJustAcceptDate=null, onlineJustAcceptDateStr=null, onlineFirstDate=null, onlineFirstDateStr=null, sourceXml=null, magXml=null, createTime=1770434672124, creator=13701087609, updateTime=1770434672124, updator=13701087609, issue=Issue{id=1226855188863038235, tenantId=1146029695717560320, journalId=1192105938417971205, year='2025', volume='65', issue='6', pageStart='2321', pageEnd='2769', issueExtLink='null', onlineDate='null', pubDate='null', beforeIssueId=null, nextIssueId=null, price=null, status=1, issueComplete=1, articleOrder=1, issueType=-1, specialIssue=0, createTime=1770434670891, creator=13701087609, updateTime=1770435273893, updator=13701087609, preIssue=null, nextIssue=null, ext={EN=IssueExt(id=1226857718103851267, tenantId=1146029695717560320, journalId=1192105938417971205, issueId=1226855188863038235, language=EN, specialIssueTitle=, coverIllustrator=null, specialIssueEditor=, specialIssueAbout=), CN=IssueExt(id=1226857718103851268, tenantId=1146029695717560320, journalId=1192105938417971205, issueId=1226855188863038235, language=CN, specialIssueTitle=, coverIllustrator=null, specialIssueEditor=, specialIssueAbout=)}, issueFiles=null}, startPage=2667, endPage=2677, ext={EN=ArticleExt(id=1226855195599094776, articleId=1226855194030425055, tenantId=1146029695717560320, journalId=1192105938417971205, language=EN, title=Interactions between chemolithoautotrophic sulfur-oxidizing bacteria and chemoheterotrophic bacteria based on carbon metabolism, columnId=1192149543992045670, journalTitle=Acta Microbiologica Sinica, columnName=Research Article, runingTitle=null, highlight=null, articleAbstract=

[Objective] To study the mechanisms of mutual promotion between chemolithoauto-trophic sulfur-oxidizing bacteria and chemoheterotrophic bacteria under co-culture based on carbon metabolism. [Methods] Ion chromatography was employed to determine the concentrations of S2O32‒ (thiosulfate) and SO42‒ (sulfate). Bacterial growth dynamics were monitored by the dilution plate method. Extracellular carbon characteristics were analyzed via total organic carbon analyzer measurement and LC-MS. Cellular morphology was observed by scanning electron microscopy. The relative mRNA levels of related genes were quantified by RT-qPCR. [Results] During the growth process, sulfur-oxidizing bacteria continuously fixed inorganic carbon and secreted organics, providing a stable carbon source for the growth of heterotrophic bacterium. In return, heterotrophic bacteria significantly enhanced the sulfur-oxidizing and carbon-fixing capabilities of sulfur-oxidizing bacteria. This was evidenced by the significantly up-regulated expression of the enzyme gene soxB involved in sulfur oxidation and the RubisCO gene cbbL involved in carbon fixation. Additionally, the production of extracellular polymeric substances was induced, which enhanced the biofilm formation. [Conclusion] This study elucidated the interaction mechanisms between sulfur-oxidizing bacteria and heterotrophic bacteria, particularly the significant enhancement of the carbon-fixing capability of sulfur-oxidizing bacteria. The findings provide a new perspective for the enrichment culture of chemolithoautotrophic bacteria and for understanding the carbon fixation mechanisms of autotrophic sulfur-oxidizing bacteria in microbial communities. Additionally, this study offers theoretical support for the low-carbon and efficient treatment of wastewater.

, correspAuthors=Weitie LIN, Jianfei LUO, authorNote=null, correspAuthorsNote=
*E-mail: LUO Jianfei,
LIN Weitie,
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【目的】 从碳代谢角度分析化能自养硫氧化细菌与化能异养细菌共培养时的相互促进作用机制。【方法】 采用离子色谱测定S2O32-和SO42-浓度，平板稀释涂布法跟踪菌体生长情况，利用总有机碳测定仪和液相色谱-质谱分析胞外碳特性，扫描电镜观察细胞形态，RT-qPCR测定相关基因表达量。【结果】 硫氧化细菌在生长过程中持续固碳，为异养细菌生长提供稳定碳源；异养细菌显著促进了硫氧化细菌的硫氧化和固碳能力，硫氧化酶基因soxB和碳固定RubisCO酶基因cbbL表达量显著增加；同时诱导产生更多的胞外聚合物，增强整体生物膜的形成。【结论】 本研究揭示了硫氧化细菌与异养细菌之间的协同作用机制，特别是异养细菌对硫氧化细菌固碳能力的显著促进作用。为化能自养细菌的富集培养及理解微生物群落中自养硫氧化细菌的固碳机制提供了新的视角，并为废水处理的低碳化和高效化提供了理论支持。

, correspAuthors=林炜铁, 罗剑飞, authorNote=null, correspAuthorsNote=null, copyrightStatement=null, copyrightOwner=null, extLink=null, articleAbsUrl=null, sourceXml=49WICyIoJMy/jE3QYRClXA==, magXml=Szczy29uvG/lI8su4LjAJw==, pdfUrl=null, pdf=kGVKpn0z21E3VCAca8gfZw==, pdfFileSize=2835781, pdfExtLink=null, richHtmlUrl=null, mobilePdfUrl=null, reviewReport=null, pdfFirstPage=null, abstractGraph=NYBDMosRm0AIO0pu0ZPk0A==, abstractGraphContent=null, abstractVideo=null, citation=null, cebUrl=null, magXmlContent=ak/VbRQZz1Pj0q/4aGsg8w==, mapNumber=null, authorCompany=null, fund=null, authors=

作者贡献声明

于晨晨：研究设计、数据处理和论文撰写；林炜铁：研究构思、论文修改；罗剑飞：研究构思、论文修改。

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A: Average consumption rate of S2O32- at different substrate concentrations; B: Changes in S2O32- and SO42- under pure culture and co-culture conditions of LS2; C: Biomass changes of LS2 in co-culture at different substrate concentrations; D: Biomass changes of Y4 in co-culture at different substrate concentrations., figureFileSmall=Y0Tda+h+iGURoqO3N2xVUg==, figureFileBig=cm+sXj4JbX5VqCK12aYDwA==, tableContent=null), ArticleFig(id=1227680961299673972, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1226855194030425055, language=CN, label=图1, caption=不同底物浓度下LS2纯培养或与Y4共培养时的硫氧化及生长特性。A：不同底物浓度下S2O32-平均消耗速率；B：LS2纯培养与共培养下S2O32-与SO42-变化；C：不同底物浓度共培养中LS2生物量变化；D：不同底物浓度共培养中Y4的生物量变化。, figureFileSmall=Y0Tda+h+iGURoqO3N2xVUg==, figureFileBig=cm+sXj4JbX5VqCK12aYDwA==, tableContent=null), ArticleFig(id=1227680961425503103, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1226855194030425055, language=EN, label=Figure 2, caption=Extracellular DOC content at different cultivation periods or conditions and its effects on the growth of Y4. A: Extracellular DOC content of LS2 at different growth stages; B: Biomass changes of Y4 utilizing extracellular DOC from LS2 at different growth stages; C: Extracellular DOC content in pure culture and co-culture of LS2 under different substrate concentrations., figureFileSmall=SAOeowWwezGXVL2DkcuDgw==, figureFileBig=icYtg9+8EnbDmxrhFOrumg==, tableContent=null), ArticleFig(id=1227680961501000581, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1226855194030425055, language=CN, label=图2, caption=不同培养时期或条件下胞外DOC含量及对Y4生长的影响。A：LS2不同生长时期胞外DOC含量；B：Y4利用LS2不同生长时期胞外DOC的生物量变化；C：不同底物浓度下LS2纯培养和共培养中胞外DOC含量。, figureFileSmall=SAOeowWwezGXVL2DkcuDgw==, figureFileBig=icYtg9+8EnbDmxrhFOrumg==, tableContent=null), ArticleFig(id=1227680961643606925, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1226855194030425055, language=EN, label=Figure 3, caption=Volcano plot of differential metabolites (A) and clustered heatmap of key differential metabolites (B)., figureFileSmall=mdxn0OdAfsqiJo+Nv6EajA==, figureFileBig=QRFH9SQ3g4D2fbgbH6kvMg==, tableContent=null), ArticleFig(id=1227680961740075925, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1226855194030425055, language=CN, label=图3, caption=差异代谢物火山图(A)与关键差异代谢物聚类热图(B), figureFileSmall=mdxn0OdAfsqiJo+Nv6EajA==, figureFileBig=QRFH9SQ3g4D2fbgbH6kvMg==, tableContent=null), ArticleFig(id=1227680961853322140, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1226855194030425055, language=EN, label=Figure 4, caption=Analysis of EPS and SEM in pure culture and co-culture. A: EPS of LS2 at different growth stages; B: Changes in EPS components in pure culture and co-culture during the stationary phase under different substrate concentrations; C: SEM of LS2 pure culture; D: SEM of LS2 and Y4 co-culture., figureFileSmall=++mAbBiy3uh/FEa9sq4Qrg==, figureFileBig=/EIYfi2rujqdSnpIyuqrwQ==, tableContent=null), ArticleFig(id=1227680961941402526, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1226855194030425055, language=CN, label=图4, caption=纯培养与共培养的EPS与SEM分析。A：LS2不同生长时期EPS含量；B：不同底物浓度下稳定期纯培养与共培养中EPS成分变化；C：LS2纯培养SEM图像；D：LS2与Y4共培养SEM图像。, figureFileSmall=++mAbBiy3uh/FEa9sq4Qrg==, figureFileBig=/EIYfi2rujqdSnpIyuqrwQ==, tableContent=null), ArticleFig(id=1227680962050454438, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1226855194030425055, language=EN, label=Figure 5, caption=Relative expression of functional genes of LS2 under pure culture and co-culture conditions., figureFileSmall=usexeUosP4bp5AZoer2lZg==, figureFileBig=RyDYWvNx88dv/pqQC9g04w==, tableContent=null), ArticleFig(id=1227680963447157678, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1226855194030425055, language=CN, label=图5, caption=纯培养与共培养条件下LS2功能基因的相对表达情况, figureFileSmall=usexeUosP4bp5AZoer2lZg==, figureFileBig=RyDYWvNx88dv/pqQC9g04w==, tableContent=null), ArticleFig(id=1227680963577181112, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1226855194030425055, language=EN, label=Table 1, caption=

Primer sequences for the target fragments

, figureFileSmall=null, figureFileBig=null, tableContent=

蛋白名称

Protein name

序列

Sequence (5′→3′)

基因名称

Gene name

GTGTCTCAGTCCCAGTGTGG

ACCTCGTGCCAAAGGATGAG

16S (LS2)
Thiosulfohydrolase SoxB

TGTGGGACAGAACGATGACG

TGGATGGTTGAAGGCTGGAC

soxB
Ribulose bisphosphate carboxylase

CCGTGCGGACTTCATTCTC

TGGTAGTGCAGGTACTGGCTC

cbbL
Type II secretion system F domain-containing protein

CGCTTTCCCTGCGGTTCA

CCTTCTTGTCGGCGTTGC

tadA
Preprotein translocase, SecA subunit

TTTCTGGGCGAAGAGTCCG

GCGTCCCTGGTATTCAAGC

secA
Lipopolysaccharide ABC transporter ATP-binding protein

GCAGGAGGCATCGGTGTT

CCAGCAGGCTTTCCAGTGTC

lptB
CDP-diacylglycerol--glycerol-3-phosphate-3-phosphatidyltransferase

CGTTGTTGGTCCTGGTGTTT

ACGATCAGCTTGTCCGCTAC

pgsA
Isocitrate dehydrogenase, NADP-dependent

AAGGTGGCTTCAAGAACTGGG

GCCGTTCAGGTTGAGGGTG

icd
4-aminobutyrate aminotransferase

TCGAGGATCAGCTCAAGCG

TCGTCCGACCGTGAAAGC

puuE
), ArticleFig(id=1227680963669455807, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1226855194030425055, language=CN, label=表1, caption=

目的片段的引物序列

, figureFileSmall=null, figureFileBig=null, tableContent=

蛋白名称

Protein name

序列

Sequence (5′→3′)

基因名称

Gene name

GTGTCTCAGTCCCAGTGTGG

ACCTCGTGCCAAAGGATGAG

16S (LS2)
Thiosulfohydrolase SoxB

TGTGGGACAGAACGATGACG

TGGATGGTTGAAGGCTGGAC

soxB
Ribulose bisphosphate carboxylase

CCGTGCGGACTTCATTCTC

TGGTAGTGCAGGTACTGGCTC

cbbL
Type II secretion system F domain-containing protein

CGCTTTCCCTGCGGTTCA

CCTTCTTGTCGGCGTTGC

tadA
Preprotein translocase, SecA subunit

TTTCTGGGCGAAGAGTCCG

GCGTCCCTGGTATTCAAGC

secA
Lipopolysaccharide ABC transporter ATP-binding protein

GCAGGAGGCATCGGTGTT

CCAGCAGGCTTTCCAGTGTC

lptB
CDP-diacylglycerol--glycerol-3-phosphate-3-phosphatidyltransferase

CGTTGTTGGTCCTGGTGTTT

ACGATCAGCTTGTCCGCTAC

pgsA
Isocitrate dehydrogenase, NADP-dependent

AAGGTGGCTTCAAGAACTGGG

GCCGTTCAGGTTGAGGGTG

icd
4-aminobutyrate aminotransferase

TCGAGGATCAGCTCAAGCG

TCGTCCGACCGTGAAAGC

puuE
), ArticleFig(id=1227680963820450761, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1226855194030425055, language=EN, label=Table 2, caption=

Differential metabolites and their metabolic pathways

, figureFileSmall=null, figureFileBig=null, tableContent=
Metabolic pathwayMetabolic pathway expression levels (%)Differential metabolites involved in the pathwayMetabolite category
Glycerophospholipid metabolism36.78

PC(O-16:0/20:3(8Z,11Z,14Z)) (A);

PE-NMe(20:1(11Z)/20:1(11Z))

[(2R)-1-[(Z)-docos-13-enoyl]oxy-3-phosphonooxypropan-2-yl] docosanoate; etc.

PC; PE; PA
Amino acids metabolism12.65

His-Gln-Val-Lys;

Leu-Ile (B); etc.

Small peptide
Glycerolipid metabolism9.20

TG(14:0/15:0/20:4(5Z,8Z,11Z,14Z));

[(2S)-1-hydroxy-3-icosanoyloxypropan-2-yl] 19-methylicosanoate 1-Oleoyl-2-acetyl-sn-glycerol (C); etc.

DG; TG
Biosynthesis of cofactors8.05Niacinamide; Arabinose-5-phosphate; etc.Alcohol or carbohydrates and amines
Biosynthesis of amino acids5.75

Dimethylglycine; Cys-Cys

histidinol (D); etc.

Amino acid derivatives;

Small peptide

Carbon metabolism5.75

2-methylene-3-methylsuccinic acid;

2-hydroxyglutarate;

Glucaric acid; etc.

FA;

Sugar acids;

Organic acid and its derivatives

TCA cycle2.30

Succinic acid semialdehyde (E);

2-hydroxyglutarate;

Glucaric acid

FA; Organic acid and its derivatives
Fatty acid metabolism or degradation2.30Carnitine C13:0 (F); 3-hydroxydecanoic acid (G); Yuzu-lactone; etc.Organic acid and its derivatives; FA; Esters
Glycolysis/Gluconeogenesis/Biosynthesis of nucleotide sugars2.30D-ribose; 2-deoxy-D-ribofuranose 5-phosphate; etc.

Carbohydrates;

Organic acid and its derivatives

), ArticleFig(id=1227680963967251407, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1226855194030425055, language=CN, label=表2, caption=

差异代谢物分类

, figureFileSmall=null, figureFileBig=null, tableContent=
Metabolic pathwayMetabolic pathway expression levels (%)Differential metabolites involved in the pathwayMetabolite category
Glycerophospholipid metabolism36.78

PC(O-16:0/20:3(8Z,11Z,14Z)) (A);

PE-NMe(20:1(11Z)/20:1(11Z))

[(2R)-1-[(Z)-docos-13-enoyl]oxy-3-phosphonooxypropan-2-yl] docosanoate; etc.

PC; PE; PA
Amino acids metabolism12.65

His-Gln-Val-Lys;

Leu-Ile (B); etc.

Small peptide
Glycerolipid metabolism9.20

TG(14:0/15:0/20:4(5Z,8Z,11Z,14Z));

[(2S)-1-hydroxy-3-icosanoyloxypropan-2-yl] 19-methylicosanoate 1-Oleoyl-2-acetyl-sn-glycerol (C); etc.

DG; TG
Biosynthesis of cofactors8.05Niacinamide; Arabinose-5-phosphate; etc.Alcohol or carbohydrates and amines
Biosynthesis of amino acids5.75

Dimethylglycine; Cys-Cys

histidinol (D); etc.

Amino acid derivatives;

Small peptide

Carbon metabolism5.75

2-methylene-3-methylsuccinic acid;

2-hydroxyglutarate;

Glucaric acid; etc.

FA;

Sugar acids;

Organic acid and its derivatives

TCA cycle2.30

Succinic acid semialdehyde (E);

2-hydroxyglutarate;

Glucaric acid

FA; Organic acid and its derivatives
Fatty acid metabolism or degradation2.30Carnitine C13:0 (F); 3-hydroxydecanoic acid (G); Yuzu-lactone; etc.Organic acid and its derivatives; FA; Esters
Glycolysis/Gluconeogenesis/Biosynthesis of nucleotide sugars2.30D-ribose; 2-deoxy-D-ribofuranose 5-phosphate; etc.

Carbohydrates;

Organic acid and its derivatives

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基于碳代谢的化能自养硫氧化细菌与化能异养细菌的相互作用
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于晨晨 , 林炜铁 * , 罗剑飞 *
微生物学报 | 研究报告 2025,65(6): 2667-2677
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微生物学报 | 研究报告 2025, 65(6): 2667-2677
基于碳代谢的化能自养硫氧化细菌与化能异养细菌的相互作用
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于晨晨, 林炜铁* , 罗剑飞*
作者信息
  • 华南理工大学 生物科学与工程学院，广东 广州
Interactions between chemolithoautotrophic sulfur-oxidizing bacteria and chemoheterotrophic bacteria based on carbon metabolism
Chenchen YU, Weitie LIN* , Jianfei LUO*
Affiliations
  • School of Biology and Biological Engineering, South China University of Technology, Guangzhou, Guangdong, China
出版时间: 2025-06-04 doi: 10.13343/j.cnki.wsxb.20250160
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摘要
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【目的】 从碳代谢角度分析化能自养硫氧化细菌与化能异养细菌共培养时的相互促进作用机制。【方法】 采用离子色谱测定S2O32-和SO42-浓度，平板稀释涂布法跟踪菌体生长情况，利用总有机碳测定仪和液相色谱-质谱分析胞外碳特性，扫描电镜观察细胞形态，RT-qPCR测定相关基因表达量。【结果】 硫氧化细菌在生长过程中持续固碳，为异养细菌生长提供稳定碳源；异养细菌显著促进了硫氧化细菌的硫氧化和固碳能力，硫氧化酶基因soxB和碳固定RubisCO酶基因cbbL表达量显著增加；同时诱导产生更多的胞外聚合物，增强整体生物膜的形成。【结论】 本研究揭示了硫氧化细菌与异养细菌之间的协同作用机制，特别是异养细菌对硫氧化细菌固碳能力的显著促进作用。为化能自养细菌的富集培养及理解微生物群落中自养硫氧化细菌的固碳机制提供了新的视角，并为废水处理的低碳化和高效化提供了理论支持。

化能自养硫氧化细菌  /  异养细菌  /  固碳能力  /  共培养

[Objective] To study the mechanisms of mutual promotion between chemolithoauto-trophic sulfur-oxidizing bacteria and chemoheterotrophic bacteria under co-culture based on carbon metabolism. [Methods] Ion chromatography was employed to determine the concentrations of S2O32‒ (thiosulfate) and SO42‒ (sulfate). Bacterial growth dynamics were monitored by the dilution plate method. Extracellular carbon characteristics were analyzed via total organic carbon analyzer measurement and LC-MS. Cellular morphology was observed by scanning electron microscopy. The relative mRNA levels of related genes were quantified by RT-qPCR. [Results] During the growth process, sulfur-oxidizing bacteria continuously fixed inorganic carbon and secreted organics, providing a stable carbon source for the growth of heterotrophic bacterium. In return, heterotrophic bacteria significantly enhanced the sulfur-oxidizing and carbon-fixing capabilities of sulfur-oxidizing bacteria. This was evidenced by the significantly up-regulated expression of the enzyme gene soxB involved in sulfur oxidation and the RubisCO gene cbbL involved in carbon fixation. Additionally, the production of extracellular polymeric substances was induced, which enhanced the biofilm formation. [Conclusion] This study elucidated the interaction mechanisms between sulfur-oxidizing bacteria and heterotrophic bacteria, particularly the significant enhancement of the carbon-fixing capability of sulfur-oxidizing bacteria. The findings provide a new perspective for the enrichment culture of chemolithoautotrophic bacteria and for understanding the carbon fixation mechanisms of autotrophic sulfur-oxidizing bacteria in microbial communities. Additionally, this study offers theoretical support for the low-carbon and efficient treatment of wastewater.

chemolithoautotrophic sulfur-oxidizing bacteria  /  heterotrophic bacteria  /  carbon-fixing capability  /  co-culture
于晨晨, 林炜铁, 罗剑飞. 基于碳代谢的化能自养硫氧化细菌与化能异养细菌的相互作用. 微生物学报, 2025 , 65 (6) : 2667 -2677 . DOI: 10.13343/j.cnki.wsxb.20250160
Chenchen YU, Weitie LIN, Jianfei LUO. Interactions between chemolithoautotrophic sulfur-oxidizing bacteria and chemoheterotrophic bacteria based on carbon metabolism[J]. Acta Microbiologica Sinica, 2025 , 65 (6) : 2667 -2677 . DOI: 10.13343/j.cnki.wsxb.20250160
正文
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化能自养硫氧化细菌通过氧化含硫化合物(S2-、S0和S2O32-)获取能量，并以CO2作为唯一碳源进行生长[1]。这一独特的代谢特性使其在环境治理中具有重要意义：一方面，硫氧化细菌能够有效去除有毒的硫化物，降低其对环境的危害；另一方面，它们通过固碳作用固定大气中的CO2，为减缓温室气体排放提供了潜在的解决方案。然而，与硫氧化细菌在去除硫化物方面的研究相比，其固碳能力的相关研究相对较少。实际上，硫氧化细菌在废水处理和工业废气净化过程中表现出显著的固碳潜力。在废水处理系统中，它们不仅能够降解高浓度的含硫污染物，还能固定大量的CO2，从而为实现“碳负排”提供了重要支持。
硫氧化细菌在氧化底物时产生的电子进入呼吸链并按照一定比例分配给O2和CO2。在细胞代谢活跃的情况下，氧化的底物越多，固定的CO2越多[2-3]；固定的碳除了用于自身细胞骨架和胞内大分子合成，还会释放到胞外。研究表明，化能自养细菌生长过程中释放到胞外的碳最高可占总固碳量的20%[4-7]，且这种胞外碳的释放对其固碳能力具有显著的反馈抑制效应[6-9]。研究表明，化能自养硝化微生物与异养细菌共培养时，异养细菌(如假单胞菌)可以利用硝化细菌释放的胞外有机物进行生长代谢，从而减少对硝化菌的细胞毒性，并促进生物膜的形成[10-11]；这些研究表明，化能自养微生物与异养微生物之间的协同作用在提高固碳效率和适应环境变化中起着重要作用。目前文献报道指出，化能自养菌释放的胞外有机物大分子以蛋白质和多糖为主，小分子则主要是分泌氨基酸和有机酸。然而，尚未有明确的研究揭示这些物质的具体分泌时期及规律。此外，目前共培养方面的研究主要集中在cbb基因上，尚未见对其他代谢途径的研究。
本研究以典型硫氧化细菌Halothiobacillusdiazotrophicus LS2[12]为研究对象，通过与伴生菌假单胞菌(Pseudomonas sp.) Y4共培养，偶联硫氧化与碳固定，分析LS2分泌的胞外碳的组成形式及规律；联合基因组与代谢组分析多种代谢途径的功能基因，系统探究二者之间基于碳代谢的作用机制。本研究为化能自养细菌的富集培养提供了新视角，有助于理解微生物群落中自养硫氧化细菌的固碳机制，同时为含硫废水处理的低碳化和高效化提供了理论支持。
1 材料与方法
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1.1 菌株和培养基
1.1.1 硫氧化细菌
Halothiobacillus diazotrophicus LS2 (=GDMCC 1.4095T=JCM 39442T)是本实验室保存的一株硫氧化细菌。菌液与甘油按1:1体积比混匀后，冻存于-70 ℃。活化时，取冻存于-70 ℃的菌株，以1%的接种量接入液体培养基中，置于30 ℃、150 r/min摇床培养2 d；随后采用稀释涂布法接种至固体培养基上，静置于30 ℃生化培养箱培养5 d，挑取单菌落接入液体培养基，即作为种子液用于后续实验。
LS2液体培养基(g/L)：MgSO4·7H2O 0.12，NaCl 1.00，CaCl2 0.01；Widdel微量元素溶液[13]：1.00 mL/L，121 ℃灭菌20 min后，加入过滤除菌的NaHCO3 0.84 g/L、NH4Cl 0.11 g/L、K2HPO4 5.23 g/L、KH2PO4 2.72 g/L、FeCl2 0.005 1 g/L，底物Na2S2O3·5H2O的添加量设置浓度梯度分别为0.25、0.50、1.00、2.00 g/L对应浓度1.00、2.00、4.00、8.00 mmol/L，固体培养基在此基础上加入琼脂粉15.00 g/L。
1.1.2 异养细菌
异养细菌假单胞菌属(Pseudomonas sp.) Y4是本实验室从硫氧化细菌富集物中分离获得。其保存和活化条件与LS2相同，液体和固体培养基均采用LB培养基。在后续的共培养实验及其纯培养对照组实验中，均采用LS2培养基。共培养中LS2和Y4的接种量比为10:1 (约105:104 CFU/mL)。Y4接种前需经8 000 r/min离心5 min，采用无菌水重悬清洗菌体，重复3次。
1.2 硫氧化菌生长特性测定
1.2.1 S2O32-和SO42-的测定
采用离子色谱法(Dionex Aquion RFIC, Dionex IonPac AS19 IC柱)测定底物S2O32-和产物SO42-的浓度。淋洗液为18 mmol/L KOH，流速1 mL/min，抑制器电流45 mA，柱温30 ℃，进样量25 μL，背景电导4-6 μS/cm。
1.2.2 生长量测定
通过稀释涂布平板法和菌落计数法跟踪测定菌体生长情况。
1.3 胞外碳测定
1.3.1 胞外可溶性有机碳(dissolved organic carbon, DOC)测定
DOC浓度测定采用总有机碳测定仪(岛津公司)。以高纯氧为载气，电炉温度680 ℃，进样量9 mL，加酸量1.5%，载气流量150 mL/min。前处理步骤如下：样品过0.45 μm滤膜，添加1%的1 mol/L盐酸调节pH至2.0-3.0，氮气吹扫20-25 min，直至测定空白培养基中C浓度小于1 mg/L。DOC中物质种类测定委托武汉迈特维尔生物科技有限公司采用LC-MS对细菌胞外代谢物进行代谢组学分析，以对数生长期后期种子液刚接种时取样过膜的样品作为对照组(CK)，培养至对数生长期后期的样品作为实验组(LS2)，并设置4次生物学重复。
1.3.2 胞外聚合物(extracellular polymeric substances, EPS)测定
采用改良后的热提法[14-15]提取胞外EPS，再分别采用BCA法测定蛋白(PN)和硫酸-蒽酮法测定糖类(PS)[16]。采用NanoDrop测定提取EPS前后溶液中DNA浓度，以确保提取EPS过程中细胞未破裂[17]。所有测定重复3次。
1.4 基因表达分析
1.4.1 RNA提取
抽滤过膜收集菌体，用高温灭菌的超纯水重悬，8 ℃、12 000 r/min离心2 min，弃上清；加入1 mL RNAiso Plus，室温静置5 min，提取RNA；加入200 μL氯仿，手摇混匀使充分乳化，静置3 min后12 000 r/min离心2 min；收集上清液至新的离心管中，加入等体积异丙醇和1 μL核酸助沉剂，充分混匀，静置10 min后12 000 r/min离心5 min，弃上清；加入1 mL 75%乙醇，充分混匀后12 000 r/min离心5 min，弃上清，室温干燥至沉淀透明色，加入适量RNase-free水溶解沉淀，得到菌株的RNA，用于下一步实验操作或置于-80 ℃冰箱保存[18]。
1.4.2 荧光定量PCR
提取的RNA按照Trans Start® One-Step gDNA Removal and cDNA Synthesis SuperMix试剂盒(北京全式金生物技术有限公司)进行反转录。将得到的cDNA按照Trans Start® Tip Green qPCR SuperMix试剂盒(北京全式金生物技术有限公司)进行反应液配制及反应程序设置，并在Light Cycler 96序列检测系统(Roche公司)中运行。引物设计采用Primer 5.0软件(表1)，引物合成由广州天一辉远基因科技有限公司完成。
1.5 扫描电子显微镜(scanning electron microscope, SEM)
收集处于对数生长期的LS2菌体和共培养混合菌体，使用10 mmol/L磷酸缓冲液(pH 7.0)润洗3遍，加入2.5%戊二醛溶液置于4 ℃冰箱中固定12 h，随后10 000 r/min离心5 min弃上清；使用30%、50%、70%、90%、100%乙醇溶液进行梯度脱水，最后将100%乙醇脱水后的菌块包裹在滤纸中，置于无水乙醇中4 ℃保存；加入过膜的100%叔丁醇，振荡，并静置20 min，再以1 000 r/min离心5 min，弃上清；样品经冷冻干燥36 h后，将干燥后的样品粉末粘在导电胶上，放置于载物台上，用镀膜仪喷金，最后使用Merlin场发射型SEM进行形态观察，加速电压为10.0 kV。
1.6 数据统计分析
所有实验(除非特别说明)均进行了3次重复。图表使用OriginPro 2025绘制，实验数据首先通过方差分析(analysis of variance, ANOVA)分析判断组间是否存在显著差异，若存在差异，则进一步采用Tukey HSD检验进行多重比较，以确定具体组间差异。统计结果中，P<0.05表示显著差异，P<0.01表示极显著差异。
2 结果与分析
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2.1 不同底物浓度下LS2与Y4共培养的硫氧化及生长特性
在常氧且碳源充足条件下，不同底物浓度下菌株LS2与Y4共培养与纯培养的硫氧化及生长特性如图1所示。与纯培养相比，除1 mmol/L底物浓度外，共培养中硫代硫酸盐的平均氧化速度在其他底物浓度下均显著提高(P<0.05)，且随着底物浓度的升高，硫氧化速率呈极显著的促进趋势(P<0.01)。例如，8 mmol/L的底物S2O32-在LS2正常代谢情况下需要32-36 h消耗完，而在共培养下只需24-28 h，其硫代硫酸盐的平均氧化速率约增加了41.5%。同时，LS2生物量测定结果(图1C)表明，共培养中LS2的生物量积累显著高于纯培养，最高可达纯培养的1.5倍。此外，如图1D所示，Y4在LS2培养基中仅能从1×104 CFU/mL生长到7×105 CFU/mL，而共培养中Y4利用硫氧化细菌LS2产生的胞外碳可生长到8×107 CFU/mL。
2.2 硫氧化细菌胞外DOC分析
为探究硫氧化细菌在不同生长时期胞外碳产生的特性及其规律，以4 mmol/L底物培养LS2并从中提取不同时期的无菌滤液，测定其中的DOC含量，结果如图2A所示。LS2从对数期到衰退期产生的DOC浓度呈逐步下降趋势，范围为6.96-9.15 mg/L，进一步将异养细菌Y4以104 CFU/mL的初始浓度接入其中，其生物量变化如图2B所示。Y4在LS2对数期滤液中表现出最高的生长量，细胞浓度可达2×108 CFU/mL，这一结果与图2A中DOC的测定结果一致，表明对数期的LS2为Y4提供最为丰富的胞外碳源，供其生长代谢。此外，图2B进一步揭示硫氧化细菌在其整个生长周期中不断产生DOC，供Y4实现有效增殖，表明硫氧化细菌的自养固碳过程是持续性的。如图2C所示，随着底物浓度的升高，LS2纯培养体系的DOC含量从6.78 mg/L显著升高到10.64 mg/L (P<0.05)。共培养体系的DOC含量则显著低于纯培养(纯培养vs.共培养：6.78→3.77 mg/L，8.97→4.31 mg/L，10.64→5.86 mg/L，P<0.01)，表明其产生的DOC可被Y4利用。通过计算发现，Y4对LS2产生的DOC利用率分别为44.3%、51.9%、44.9%。上述结果表明，底物浓度对硫氧化细菌胞外DOC释放及异养细菌的利用均具有一定影响，且二者并不呈简单的线性相关。
2.3 硫氧化细菌胞外碳LC-MS分析
对LS2对数生长期后期产生胞外DOC进行基于LC-MS的代谢组学分析。LC-MS共检测出1 240种物质，基于OPLS-DA模型得到的变量重要性投影(VIP)，结合单变量分析的P-value/FDR。选取VIP>1且P-value<0.05的代谢物，认为其差异显著。检测出差异代谢物228种，其中上调的有131种。构成生物膜成分的甘油磷脂(glycerophosphatide, GP)、甘油酯(glyceride, GL)和脂肪酸(fatty acid, FA)所占比例最高，达32.82%，可能参与能量代谢的有机酸及其衍生物占比14.50%，氨基酸及其代谢物和碳水化合物共占比11.45% (图3A)。表2展示了不同代谢途径的表达量以及参与该途径的差异代谢物(图3A中字母编号与表中相对应)。其中表达量占比最高的为甘油磷脂代谢，主要功能是参与群体感应或生物膜的合成，参与表达的差异代谢物类别多为磷脂酰胆碱(phosphatidylcholine, PC)、磷脂酰乙醇胺(phosphatidyl ethanolamine, PE)和磷脂酸(phosphatidic acid, PA)，且大多数为上调表达，相对定量趋势如图3B；其次是氨基酸的代谢和合成，参与的差异代谢物多为氨基酸衍生物和小肽分子；此外，还有同样参与生物膜和能量合成的甘油脂代谢和脂肪酸代谢，参与的差异代谢物类别分别为甘油二酯(diglyceride, DG)和甘油三酯(triglyceride, TG)，以及有机酸、脂肪酸等；最后，碳代谢、糖代谢以及辅因子合成也有一定表达量，参与的差异代谢物较少。例如，阿拉伯糖5-磷酸可能参与核苷酸和辅酶(如NAD⁺、FAD)的合成；2-羟基戊二酸可能与TCA循环中间体α-酮戊二酸的合成相关；琥珀酸半醛可能转化为琥珀酸间接参与TCA循环或参与谷氨酸代谢合成血红素。
2.4 硫氧化细菌EPS分析
以4 mmol/L底物浓度培养LS2，从中提取不同时期的EPS，测定其中的PN与PS含量，结果如图4A所示。与DOC分泌规律不同，EPS产生最多的时期是稳定期，PN浓度约为4.34 mg/L，PS浓度约为0.73 mg/L。进一步分别测定稳定期的纯培养LS2与共培养的EPS分泌情况，结果如图4B所示。在低底物浓度下，共培养EPS中的PN浓度显著增加，约为纯培养的1.62倍；在高底物浓度下，共培养EPS中的PS浓度显著增加，约为纯培养的1.15倍，表明异养细菌的存在可能增强了整体的生物膜形成。结合图4C (纯培养LS2)和图4D (LS2与Y4共培养)的SEM图像，可以明显看到共培养条件下会产生较多的胞外物质。
2.5 共培养中硫氧化细菌基因表达分析
根据2.3节LC-MS测定结果，结合本课题组在NCBI数据库中上传的LS2基因组信息，对生物膜形成、氨基酸代谢、糖代谢以及能量代谢过程中的关键酶基因设计了特异性引物进行进一步分析。以内参基因16S rRNA为对照，在共培养条件下，LS2中多个关键基因表达水平显著上调(P<0.05)。如图5所示，硫氧化过程关键基因soxB (硫氧化酶)上调11.75%，固碳过程关键基因cbbL (核酮糖-1,5-二磷酸羧化酶)上调28.04%，参与蛋白质跨膜转运的基因secA (蛋白转移酶)上调261.26%，革兰氏阴性菌细胞外膜脂多糖运输基因lptB (脂多糖转移酶)[19]上调54.17%，磷脂合成的肯尼迪途径中关键基因pgsA (磷脂酰甘油磷酸合成酶)上调91.24%，三羧酸循环中参与能量代谢和碳骨架合成的基因icd (异柠檬酸脱氢酶)上调22.65%，参与氨基酸代谢与转化的基因puuE (氨基转移酶)上调18.40%。这些结果表明在共培养条件下，Y4通过多种途径促进了LS2的生物合成及代谢反应，包括硫氧化、固碳以及生物膜形成等重要生理过程。
3 讨论与结论
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化能自养微生物因其独特的代谢策略和环境适应性，在CO₂减排与资源化方面具有重要意义。作为典型的自养硫氧化细菌，菌株LS2通过化能自养代谢实现CO₂固定，并分泌胞外碳作为异养菌的碳源，避免了传统废水处理系统中外部碳源的添加，从而降低了碳排放。LS2主要通过分泌DOC作为Y4的碳源供其生长，并在整个生长周期中持续提供碳源，表现出其作为初级生产力的特性。分泌的DOC不仅用于招募异养细菌，还可解除小分子有机物(如氨基酸、有机酸)对自身的细胞毒性[20-23]。此外，底物浓度(S2O32‒)对LS2的固碳效率也有显著影响。在低底物浓度下，游离有机碳的负反馈抑制作用更为显著[22]。本研究中，提高底物浓度后分泌的DOC和EPS量显著增加，但Y4对DOC的利用率与底物浓度之间并不呈正线性相关，可能是由于Y4对高SO42‒环境存在阈值限制，或者由于EPS的增加阻碍了其对内部DOC的摄取。此外，在共培养中，Y4可以反哺LS2，促进其硫氧化速率、生物量积累、固碳效率以及EPS的形成。EPS可以解除金属离子毒性[24]，实现对污染物的有效去除，并作为生物膜的结构基质增强微生物的耐受性，帮助其在极端环境下生存[25]。
LS2分泌的DOC主要成分是甘油酯和磷脂类物质，其表达量最高的代谢通路也是甘油酯与甘油磷脂代谢。这些物质对解除小分子有机物的抑制作用较弱，其主要功能更可能是促进生物膜的形成。研究表明在氨氧化细菌与假单胞菌的共培养中，氨氧化细菌的生物膜处于下层，而异养细菌的生物膜在上层且占95%[10]。因此，Y4可能会产生更多的生物膜并将LS2包裹在内部，形成保护屏障，避免其受到毒害作用，从而使其生长代谢正常进行。从分子层面来看，结合基因组针对各个代谢过程的关键酶设计特异性引物，进行相对基因表达分析，在共培养中不仅soxB、cbbL基因上调，与生物膜中蛋白转运secA、多糖运输lptB以及磷脂形成pgsA相关的基因表达量也显著增加。这表明代谢协同性可能是微生物细胞之间物质交换的增加导致某种代谢重排[26]。研究表明异养生物与厌氧氨氧化细菌通过群体感应(quorum sensing, QS)系统相互作用[27]。细菌生物膜的形成依赖于QS信号调控，大部分革兰氏阴性菌的QS系统为LuxI/LuxR型系统，LuxI编码合成酰基高丝氨酸内酯(acyl-homoserine lactones, AHL)信号分子。假单胞菌中的LasI与LuxI具有同源性，其编码的N-3-氧十二烷酰-高丝氨酸内酯是典型的生物膜调控信号[28]。因此，在LS2与Y4的共培养中，代谢重排很可能由QS信号分子驱动，而非简单的物质交换。即可能是Y4产生的AHL类代谢物作为QS系统的信号分子，激活了硫氧化细菌相关基因的表达。此外，icd基因的上调表明，充足的能量供给也有利于LS2的自养生长及CO2同化[22]。
自养菌分泌胞外碳具有种间特异性，不同细菌分泌的DOC成分和含量可能会有所不同。然而，与异养菌相比，自养菌的共同特点是生长缓慢，生物膜发育缓慢，而异养菌因其代谢特性会产生比自养细菌更多的胞外物质形成生物膜，并聚集在外层形成保护。这种生物膜的保护机制理论可以广泛应用于所有化能自养细菌。这可能是化能自养细菌与异养菌相互作用的普遍机制，也解释了为什么化能自养细菌难以富集纯化。此外，自养-异养共培养体系在处理高硫废水时能够实现硫化物的高效氧化和有机物的同步降解，同时减少了对外加碳源的依赖。未来可以进一步聚焦其在动态环境下的菌群互作机制，并开发三维电极生物膜反应器等新型装置，以强化硫氧化效率与碳固定能力，为工业废水低碳化处理提供依据，助力实现碳负排。
作者利益冲突公开声明
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作者声明绝无任何可能会影响本文所报告工作的已知经济利益或个人关系。
基金
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  • 国家自然科学基金(91951118)
  • 广东省自然科学基金(2025A1515011043)
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2025年第65卷第6期
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doi: 10.13343/j.cnki.wsxb.20250160
  • 接收时间：2025-02-28
  • 首发时间：2026-02-07
  • 出版时间：2025-06-04
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  • 收稿日期：2025-02-28
  • 录用日期：2025-03-14
基金
National Natural Science Foundation of China(91951118)
国家自然科学基金(91951118)
Guangdong Basic and Applied Basic Research Foundation(2025A1515011043)
广东省自然科学基金(2025A1515011043)
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    华南理工大学 生物科学与工程学院，广东 广州

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2种不同金属材料的力学参数
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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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