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Article(id=1226554101543121011, tenantId=1146029695717560320, journalId=1192105938417971205, issueId=1226554095926952065, articleNumber=null, orderNo=null, doi=10.13343/j.cnki.wsxb.20240833, pmid=null, cstr=null, oa=null, hot=null, price=null, onlineType=0, articleFormat=0, articleType=null, articleTypeStr=research-article, receivedDate=1734624000000, receivedDateStr=2024-12-20, revisedDate=null, revisedDateStr=null, acceptedDate=1736179200000, acceptedDateStr=2025-01-07, onlineDate=1770362886081, onlineDateStr=2026-02-06, pubDate=1751558400000, pubDateStr=2025-07-04, doiRegisterDate=null, doiRegisterDateStr=null, onlineIssueDate=1770362886081, onlineIssueDateStr=2026-02-06, onlineJustAcceptDate=null, onlineJustAcceptDateStr=null, onlineFirstDate=null, onlineFirstDateStr=null, sourceXml=null, magXml=null, createTime=1770362886081, creator=13701087609, updateTime=1770362886081, updator=13701087609, issue=Issue{id=1226554095926952065, tenantId=1146029695717560320, journalId=1192105938417971205, year='2025', volume='65', issue='7', pageStart='2771', pageEnd='3233', issueExtLink='null', onlineDate='null', pubDate='null', beforeIssueId=null, nextIssueId=null, price=null, status=1, issueComplete=1, articleOrder=1, issueType=-1, specialIssue=null, createTime=1770362884741, creator=13701087609, updateTime=1770363575040, updator=13701087609, preIssue=null, nextIssue=null, ext={EN=IssueExt(id=1226556991309529548, tenantId=1146029695717560320, journalId=1192105938417971205, issueId=1226554095926952065, language=EN, specialIssueTitle=, coverIllustrator=null, specialIssueEditor=, specialIssueAbout=), CN=IssueExt(id=1226556991309529549, tenantId=1146029695717560320, journalId=1192105938417971205, issueId=1226554095926952065, language=CN, specialIssueTitle=, coverIllustrator=null, specialIssueEditor=, specialIssueAbout=)}, issueFiles=null}, startPage=3041, endPage=3055, ext={EN=ArticleExt(id=1226554101853499533, articleId=1226554101543121011, tenantId=1146029695717560320, journalId=1192105938417971205, language=EN, title=Biological characteristics and genome sequences of two bacteriophage strains infecting Stenotrophomonas indicatrix, columnId=1192149543992045670, journalTitle=Acta Microbiologica Sinica, columnName=Research Article, runingTitle=null, highlight=null, articleAbstract=

[Objective] Stenotrophomonas can promote the growth of plants and aquatic algae. However, limited studies have focused on the bacteriophages infecting Stenotrophomonas. In this study, we isolated bacteriophages infecting Stenotrophomonas from water and studied their biological and genomic characteristics, aiming to improve our understanding of the ecological functions of Stenotrophomonas and its bacteriophages. [Methods] The double-layer plate method was employed to isolate bacteriophages infecting S. indicatrix EB12 from lake water. The biological characteristics, whole genome sequence characteristics, gene functions, phylogenetic relationship, and protein structures of the isolates were analyzed. [Results] Transmission electron microscopy showed that two isolates Ste-X and Ste-D were short-tailed bacteriophages. The incubation period of both strains was 20 min. Ste-X and Ste-D showed the optimal multiplicities of infection being 1 000 and 10, burst sizes of 28.8 PFU/cell and 131.1 PFU/cell, temperature tolerance ranges of 20-60 °C and 20-70 °C, and pH tolerance ranges of pH 4.0-13.0 and pH 3.0-12.0, respectively. Ste-X and Ste-D were deactivated by UV irradiation for 60 min and 120 min, respectively. Their host ranges were narrow. The genomes of both strains showed the lengths of 39 429 bp, with the G+C content of 57.80% and 57.85%, respectively, and both of them contained 65 open reading frames (ORFs). The genomes of the two strains contained only three different bases. However, their homology with other bacteriophages was low, which suggested that the two strains were novel short-tailed bacteriophages. The structures of the proteins encoded by ORF34 and ORF52 were predicted. Result showed thant the proteins encoded by ORF34 were acidic, stable, and hydrophilic, containing two conserved domains, ChtBD3 and PHA00661, with the three-dimensional structures dominated by random coils. The proteins encoded by ORF52 were alkaline, unstable, hydrophilic, with no conserved domain and the three-dimensional structures dominated by α-helixes. [Conclusion] Two novel strains of short-tailed bacteriophages with high genome similarity but distinct biological characteristics were isolated from water.

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*E-mail: JING Ruiyong,
LIU Junjie,
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【目的】 寡养单胞菌(Stenotrophomonas)对植物和水体藻类具有促生效果，但目前关于寡养单胞菌噬菌体的相关研究报道较少。本研究从水体中分离侵染寡养单胞菌的噬菌体，并对其生物学及基因组特征进行研究，有助于加强对寡养单胞菌及其噬菌体生态功能的理解。 【方法】 以蓝藻附生细菌指示器寡养单胞菌(S. indicatrix) EB12为宿主，采用双层平板法从湖水中分离噬菌体，并对其生物学特性、全基因组序列特征、基因功能注释、系统进化及蛋白质结构进行分析。 【结果】 透射电镜显示，分离获得的2株噬菌体Ste-X和Ste-D均为短尾噬菌体；其潜伏期均为20 min；最佳感染复数分别为1 000和10；裂解量分别为28.8 PFU/cell和131.1 PFU/cell；温度耐受范围分别为20-60 ℃和20-70 ℃；pH耐受范围分别为pH 4.0-13.0和pH 3.0-12.0；在紫外照射下，Ste-X和Ste-D分别于60 min和120 min后失活，且宿主范围较窄；2株噬菌体的基因组长度均为39 429 bp，G+C含量分别为57.80%和57.85%，均含有65个开放阅读框(open reading frame, ORF)，2株噬菌体仅含3个差异碱基，但与其他噬菌体的同源性较低，均为新的短尾噬菌体。对差异碱基所在的开放阅读框ORF34和ORF52所编码的蛋白质结构进行预测分析，结果显示，ORF34编码的蛋白质均为酸性、稳定的亲水蛋白，均含有ChtBD3和PHA00661这2个保守结构域，其空间结构以无规则卷曲为主；ORF52编码的蛋白质均为碱性、不稳定的亲水蛋白，无保守结构域，空间结构以α螺旋为主。 【结论】 从水体中分离得到2株全基因组高度相似但生物学特性明显不同的新型短尾噬菌体。

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作者贡献声明

姜雪：开展实验，数据分析及文章撰写与修改；夏玉侨：开展实验，数据分析；王丽艳：数据分析和文章修改；李喜梅：数据分析和文章修改；荆瑞勇：试验设计、数据处理及文章修改；刘俊杰：试验设计、数据处理及文章修改。

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Frontiers in Microbiology, 2022, 12: 754331., articleTitle=First characterization of a Hafnia phage reveals extraordinarily large burst size and unusual plaque polymorphism, refAbstract=null), Reference(id=1227681745512886995, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1226554101543121011, doi=null, pmid=null, pmcid=null, year=2018, volume=809, issue=null, pageStart=13, pageEnd=19, url=null, language=null, rfNumber=[40], rfOrder=47, authorNames=AN ML, ZHENG Z, QU CF, WANG XX, CHEN H, SHI CL, MIAO JL, journalName=Mutation Research-Fundamental and Molecular Mechanisms of Mutagenesis, refType=null, unstructuredReference=AN ML, ZHENG Z, QU CF, WANG XX, CHEN H, SHI CL, MIAO JL. The first (6-4) photolyase with DNA damage repair activity from the Antarctic microalga Chlamydomonas sp. ICE-L[J]. Mutation Research-Fundamental and Molecular Mechanisms of Mutagenesis, 2018, 809: 13-19., articleTitle=The first (6-4) photolyase with DNA damage repair activity from the Antarctic microalga Chlamydomonas sp. ICE-L, refAbstract=null), Reference(id=1227681745617744597, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1226554101543121011, doi=null, pmid=null, pmcid=null, year=1997, volume=63, issue=4, pageStart=1551, pageEnd=1556, url=null, language=null, rfNumber=[41], rfOrder=48, authorNames=FURUTA M, SCHRADER JO, SCHRADER HS, KOKJOHN TA, NYAGA S, McCULLOUGH AK, LLOYD RS, BURBANK DE, LANDSTEIN D, LANE L, van ETTEN JL, journalName=Applied and Environmental Microbiology, refType=null, unstructuredReference=FURUTA M, SCHRADER JO, SCHRADER HS, KOKJOHN TA, NYAGA S, McCULLOUGH AK, LLOYD RS, BURBANK DE, LANDSTEIN D, LANE L, van ETTEN JL. Chlorella virus PBCV-1 encodes a homolog of the bacteriophage T4 UV damage repair gene denV[J]. 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A: Hydrophilicity and hydrophobicity of ORF34 protein from Ste-D; B: Hydrophilicity and hydrophobicity of ORF34 protein from Ste-X; C: Hydrophilicity and hydrophobicity of ORF52 protein from Ste-D; D: Hydrophilicity and hydrophobicity of ORF52 protein from Ste-X., figureFileSmall=wgLcuIjBl1WAJU271J5G+g==, figureFileBig=kGw0Ca9k1Dt2qUSRfH39iw==, tableContent=null), ArticleFig(id=1227681736134422906, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1226554101543121011, language=CN, label=图6, caption=两株噬菌体ORF34和ORF52蛋白的亲疏水性, figureFileSmall=wgLcuIjBl1WAJU271J5G+g==, figureFileBig=kGw0Ca9k1Dt2qUSRfH39iw==, tableContent=null), ArticleFig(id=1227681736285417863, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1226554101543121011, language=EN, label=Figure 7, caption=Secondary structure prediction of ORF34 and ORF52 proteins of two phages (A) and prediction of the tertiary structure of ORF34 protein of Ste-D (B) and Ste-X (C)., figureFileSmall=WRiRyj+hj4aTSFKrxrzY7A==, figureFileBig=pfOknNhVMjYjpdPQ1XOwxg==, tableContent=null), ArticleFig(id=1227681736411246987, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1226554101543121011, language=CN, label=图7, caption=两株噬菌体ORF34和ORF52蛋白的二级结构预测(A)和ORF34蛋白的三级结构预测(B、C), figureFileSmall=WRiRyj+hj4aTSFKrxrzY7A==, figureFileBig=pfOknNhVMjYjpdPQ1XOwxg==, tableContent=null), ArticleFig(id=1227681736537076115, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1226554101543121011, language=EN, label=Table 1, caption=

Multiplicity of infection of phage Ste-X and Ste-D

, figureFileSmall=null, figureFileBig=null, tableContent=
PhageMultiplicity of infection (MOI)

Phage concertration

(PFU/mL)

Bacteria concertration (CFU/mL)Phage titer (PFU/mL)
Ste-X10 0001071031.27×107
1 0001071041.57×107
1001071051.47×107
101071066.67×106
11071074.89×106
0.11071085.56×105
0.011061082.11×104
Ste-D10 00010101062.49×108
1 00010101073.03×109
10010101083.27×109
101091084.10×1010
11081082.46×1010
0.11071081.41×109
0.011061087.89×108
), ArticleFig(id=1227681736662905243, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1226554101543121011, language=CN, label=表1, caption=

噬菌体Ste-X和Ste-D的最佳感染复数

, figureFileSmall=null, figureFileBig=null, tableContent=
PhageMultiplicity of infection (MOI)

Phage concertration

(PFU/mL)

Bacteria concertration (CFU/mL)Phage titer (PFU/mL)
Ste-X10 0001071031.27×107
1 0001071041.57×107
1001071051.47×107
101071066.67×106
11071074.89×106
0.11071085.56×105
0.011061082.11×104
Ste-D10 00010101062.49×108
1 00010101073.03×109
10010101083.27×109
101091084.10×1010
11081082.46×1010
0.11071081.41×109
0.011061087.89×108
), ArticleFig(id=1227681736771957155, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1226554101543121011, language=EN, label=Table 2, caption=

The host range of phage Ste-X and Ste-D

, figureFileSmall=null, figureFileBig=null, tableContent=
StrainsSte-XSte-D
Pseudomonas alcaliphila EB17--
Pseudomonas sediminis EB8++
Pseudomonas guguanensis EB4--
Stutzerimonas stutzeri L4.6--
Stenotrophomonas nematodicola EB23--
Stenotrophomonas indicatrix EB12\\
Pseudomonas hibiscicola N5.33--
Rhizobium rosettiformans L4.22--
Tsukamurella pulmonis L5.29--
Sphingobacterium soli EB19--
), ArticleFig(id=1227681736893591977, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1226554101543121011, language=CN, label=表2, caption=

噬菌体Ste-X和Ste-D的宿主范围

, figureFileSmall=null, figureFileBig=null, tableContent=
StrainsSte-XSte-D
Pseudomonas alcaliphila EB17--
Pseudomonas sediminis EB8++
Pseudomonas guguanensis EB4--
Stutzerimonas stutzeri L4.6--
Stenotrophomonas nematodicola EB23--
Stenotrophomonas indicatrix EB12\\
Pseudomonas hibiscicola N5.33--
Rhizobium rosettiformans L4.22--
Tsukamurella pulmonis L5.29--
Sphingobacterium soli EB19--
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两株侵染寡养单胞菌噬菌体的生物学特性及全基因组分析
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姜雪 1, 2 , 夏玉侨 1 , 王丽艳 1 , 李喜梅 1 , 荆瑞勇 1 , 刘俊杰 2
微生物学报 | 研究报告 2025,65(7): 3041-3055
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微生物学报 | 研究报告 2025, 65(7): 3041-3055
两株侵染寡养单胞菌噬菌体的生物学特性及全基因组分析
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姜雪1, 2, 夏玉侨1, 王丽艳1, 李喜梅1, 荆瑞勇1 , 刘俊杰2
作者信息
  • 1.黑龙江八一农垦大学 生命科学技术学院，黑龙江省寒区环境微生物与农业废弃物资源化利用重点实验室，黑龙江 大庆
  • 2.中国科学院东北地理与农业生态研究所，黑土区农业生态重点实验室，黑龙江 哈尔滨
Biological characteristics and genome sequences of two bacteriophage strains infecting Stenotrophomonas indicatrix
Xue JIANG1, 2, Yuqiao XIA1, Liyan WANG1, Ximei LI1, Ruiyong JING1 , Junjie LIU2
Affiliations
  • 1.Heilongjinag Provincal Key Laboratory of Environmental Microbiology and Recycling of Agro-waste in Cold Region, College of Life Science and Biotechnology, Heilongjiang Bayi Agricultural University, Daqing, Heilongjiang, China
  • 2.Key Laboratory of Mollisols Agroecology, Northeast Institute of Geography and Agroecology, Chinese Academy of Sciences, Harbin, Heilongjiang, China
出版时间: 2025-07-04 doi: 10.13343/j.cnki.wsxb.20240833
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摘要
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【目的】 寡养单胞菌(Stenotrophomonas)对植物和水体藻类具有促生效果，但目前关于寡养单胞菌噬菌体的相关研究报道较少。本研究从水体中分离侵染寡养单胞菌的噬菌体，并对其生物学及基因组特征进行研究，有助于加强对寡养单胞菌及其噬菌体生态功能的理解。 【方法】 以蓝藻附生细菌指示器寡养单胞菌(S. indicatrix) EB12为宿主，采用双层平板法从湖水中分离噬菌体，并对其生物学特性、全基因组序列特征、基因功能注释、系统进化及蛋白质结构进行分析。 【结果】 透射电镜显示，分离获得的2株噬菌体Ste-X和Ste-D均为短尾噬菌体；其潜伏期均为20 min；最佳感染复数分别为1 000和10；裂解量分别为28.8 PFU/cell和131.1 PFU/cell；温度耐受范围分别为20-60 ℃和20-70 ℃；pH耐受范围分别为pH 4.0-13.0和pH 3.0-12.0；在紫外照射下，Ste-X和Ste-D分别于60 min和120 min后失活，且宿主范围较窄；2株噬菌体的基因组长度均为39 429 bp，G+C含量分别为57.80%和57.85%，均含有65个开放阅读框(open reading frame, ORF)，2株噬菌体仅含3个差异碱基，但与其他噬菌体的同源性较低，均为新的短尾噬菌体。对差异碱基所在的开放阅读框ORF34和ORF52所编码的蛋白质结构进行预测分析，结果显示，ORF34编码的蛋白质均为酸性、稳定的亲水蛋白，均含有ChtBD3和PHA00661这2个保守结构域，其空间结构以无规则卷曲为主；ORF52编码的蛋白质均为碱性、不稳定的亲水蛋白，无保守结构域，空间结构以α螺旋为主。 【结论】 从水体中分离得到2株全基因组高度相似但生物学特性明显不同的新型短尾噬菌体。

寡养单胞菌  /  噬菌体  /  生物学特性  /  基因组

[Objective] Stenotrophomonas can promote the growth of plants and aquatic algae. However, limited studies have focused on the bacteriophages infecting Stenotrophomonas. In this study, we isolated bacteriophages infecting Stenotrophomonas from water and studied their biological and genomic characteristics, aiming to improve our understanding of the ecological functions of Stenotrophomonas and its bacteriophages. [Methods] The double-layer plate method was employed to isolate bacteriophages infecting S. indicatrix EB12 from lake water. The biological characteristics, whole genome sequence characteristics, gene functions, phylogenetic relationship, and protein structures of the isolates were analyzed. [Results] Transmission electron microscopy showed that two isolates Ste-X and Ste-D were short-tailed bacteriophages. The incubation period of both strains was 20 min. Ste-X and Ste-D showed the optimal multiplicities of infection being 1 000 and 10, burst sizes of 28.8 PFU/cell and 131.1 PFU/cell, temperature tolerance ranges of 20-60 °C and 20-70 °C, and pH tolerance ranges of pH 4.0-13.0 and pH 3.0-12.0, respectively. Ste-X and Ste-D were deactivated by UV irradiation for 60 min and 120 min, respectively. Their host ranges were narrow. The genomes of both strains showed the lengths of 39 429 bp, with the G+C content of 57.80% and 57.85%, respectively, and both of them contained 65 open reading frames (ORFs). The genomes of the two strains contained only three different bases. However, their homology with other bacteriophages was low, which suggested that the two strains were novel short-tailed bacteriophages. The structures of the proteins encoded by ORF34 and ORF52 were predicted. Result showed thant the proteins encoded by ORF34 were acidic, stable, and hydrophilic, containing two conserved domains, ChtBD3 and PHA00661, with the three-dimensional structures dominated by random coils. The proteins encoded by ORF52 were alkaline, unstable, hydrophilic, with no conserved domain and the three-dimensional structures dominated by α-helixes. [Conclusion] Two novel strains of short-tailed bacteriophages with high genome similarity but distinct biological characteristics were isolated from water.

Stenotrophomonas  /  bacteriophage  /  biological characteristics  /  genome
姜雪, 夏玉侨, 王丽艳, 李喜梅, 荆瑞勇, 刘俊杰. 两株侵染寡养单胞菌噬菌体的生物学特性及全基因组分析. 微生物学报, 2025 , 65 (7) : 3041 -3055 . DOI: 10.13343/j.cnki.wsxb.20240833
Xue JIANG, Yuqiao XIA, Liyan WANG, Ximei LI, Ruiyong JING, Junjie LIU. Biological characteristics and genome sequences of two bacteriophage strains infecting Stenotrophomonas indicatrix[J]. Acta Microbiologica Sinica, 2025 , 65 (7) : 3041 -3055 . DOI: 10.13343/j.cnki.wsxb.20240833
正文
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寡养单胞菌(Stenotrophomonas)隶属于变形菌门(Pseudomonadota)溶杆菌科(Lysobacteraceae)的一类革兰氏阴性好氧菌[1]。其中，嗜麦芽寡养单胞菌(S. maltophilia)作为人类和动物的条件致病菌被广泛研究，从土壤、植物体内等环境中分离的其他寡养单胞菌均未被检测出致病潜力，且在修复污染土壤[2]、降解有机物[3]、促进植物生长[4]、保护植株抵抗重金属污染[5]及其他逆境胁迫[6]等方面发挥着重要作用。此外，水体中也广泛存在寡养单胞菌，它可降解微囊藻毒素[7]，进而使藻类的生长不再受毒素抑制，这也是导致蓝藻水华暴发的原因之一。Fakhimi等[8]从被污染的微藻中分离得到一株寡养单胞菌(S. goyi)，该菌通过与其他微生物建立代谢网络，维持联合制氢能力进而影响微藻的生长。Lara-Moreno等[9]分离到一株S. indicatrix CPHE1，该菌可矿化土壤中的菲。本课题组在从湖水蓝藻分离过程中获得一株对蓝藻具有促生效果的附着细菌S. indicatrix EB12，它具有使水中藻类大量繁殖的潜力，威胁水生生态系统和公共健康。因此，如何通过噬菌体裂解细菌进而抑制藻华现象的发生还有待深入研究。
噬菌体(bacteriophage)是一类能够侵袭原核生物的病毒，通过与宿主互作干扰宿主代谢，烈性噬菌体可裂解宿主致其死亡[10]。噬菌体在调控生物多样性、物质循环及微生物间基因转移中发挥着重要作用[11]。目前，寡养单胞菌噬菌体的研究大多集中在S. maltophilia噬菌体[12-13]，而以指示器寡养单胞菌(S. indicatrix)为宿主的噬菌体未见报道。宏基因组研究发现，噬菌体在核苷酸序列水平上具有多样性，而构成它们的病毒粒子结构蛋白却表现出很强的相似性和保守性[14]。然而一个核苷酸位点的突变可能会使单个基因模块的功能发生变化进而影响噬菌体的生长特性及感染能力[15]。因此，突变基因模块的分析更便于明确噬菌体基因组中功能基因的注释。
水体藻际存在促生细菌，使藻类大量繁殖，从而导致水华。分离促生细菌噬菌体，可削弱水体藻类的生长。明确噬菌体的生物学特性及基因组信息，有助于加强对噬菌体及其宿主功能的理解。基于此，本研究以具有促进藻类生长的S. indicatrix EB12为宿主，从湖水中分离纯化出2株指示器寡养单胞菌(S. indicatrix)噬菌体，并从生物学特性、基因组特征及部分蛋白的预测和分析等方面拓宽了寡养单胞菌噬菌体的生物信息库，为噬菌体与寡养单胞菌调节水生生态系统提供基础资料。
1 材料与方法
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1.1 宿主菌和噬菌体来源
指示器寡养单胞菌(S. indicatrix) EB12由黑龙江八一农垦大学生命科学技术学院农业与环境微生物实验室在富集蓝藻过程中分离并保存。噬菌体Ste-X和Ste-D分离自黑龙江八一农垦大学人工湖(46°35′N, 125°10′E)采集的水样。
1.2 供试培养基及缓冲液
NA培养基(g/L)：牛肉膏3.000，蛋白胨10.000，NaCl 5.000，蒸馏水定容至1 L，pH 7.2-7.4，121 ℃灭菌30 min。SM缓冲液(g/L)：NaCl 5.800，MgSO4·7H2O 1.968，Tris-HCl 6.057，丙三醇62.500 µL，pH 7.0，121 ℃灭菌20 min。KCl溶液(g/L)：KCl 74.551，121 ℃灭菌20 min。
1.3 噬菌体的分离纯化
根据赵欣卓等[16]的方法分离纯化噬菌体。首先对采集的水样进行离心，并通过0.22 µm滤膜过滤以去除部分生物及非生物因素，以此滤液为病毒悬液。取0.3 mL病毒悬液与0.2 mL处于对数生长期(OD600值为0.8，以下所有实验使用的菌液OD600值均为0.8)的S. indicatrix EB12菌液于试管中静置1 h。采用双层平板法分离噬菌体，挑取单个大小不同的噬菌斑分别置于装有NA液体培养基的EP管中，4 ℃冰箱静置24 h以浸出病毒液，再用双层平板法纯化噬菌体，重复纯化5次以上，直至观察到噬菌斑大小均匀，即获得纯化的噬菌体。
1.4 噬菌体的浓缩与电镜观察
根据赵欣卓等[16]的方法获得病毒浓缩液，并由成都世纪美扬科技有限公司采用透射电子显微镜对噬菌体进行形态观察。
1.5 噬菌体最佳感染复数
将宿主菌EB12菌液与噬菌体分别按感染复数(multiplicity of infection, MOI)为10 000、1 000、100、10、1、0.1、0.01混合，具体操作参考赵欣卓等[16]的方法。采用双层平板法测定其效价，以无菌水为空白对照，所有试验均重复3次，最终确定最佳感染复数。
1.6 噬菌体一步生长曲线、酸碱、温度及紫外光稳定性
根据赵欣卓等[16]的方法测定噬菌体一步生长曲线。从0 min开始，每隔10 min取出100 μL混合液，采用双层平板法测定其效价并绘制一步生长曲线，如公式(1)所示。
裂解量=裂解末期噬菌体效价/感染初期宿主菌浓度
取10 μL噬菌体原液分别加入0.99 mL不同pH 3.0-13.0的NA液体培养基中，采用双层平板法测定其效价；取2 mL噬菌体原液，分别置于20-80 ℃的恒温水浴锅中孵育1 h后测定其效价；取10 mL噬菌体原液分别置于3个90 mm无菌平皿中，置于紫外灯(30 W)下30 cm处进行照射，每10 min取样1次测定其效价。以上所有试验均重复3次。
1.7 噬菌体的宿主范围
供试宿主菌为本实验室从大庆湿地水体蓝藻分离获得的附生细菌共9株，分别为嗜碱假单胞菌(Pseudomonas alcaliphila) EB17、P. sediminis EB8、谷关假单胞菌(P. guguanensis) EB4、施氏施蒂泽氏单胞菌(Stutzerimonas stutzeri) L4.6、S. nematodicola EB23、栖木槿假单胞菌(P. hibiscicola) N5.33、花结状根瘤菌(Rhizobium rosettiformans) L4.22、肺冢村氏菌(Tsukamurella pulmonis) L5.29、土地鞘氨醇杆菌(Sphingobacterium soli) EB19。
向0.2 mL宿主菌液中加入6 mL预热的NA半固体培养基，混合均匀后立即倒入已凝固的NA固体培养基上。待培养基完全凝固后，取2 μL病毒液进行点样，待病毒液晾干后于30 ℃培养箱中倒置培养，24-48 h后观察是否形成噬菌斑。
1.8 噬菌体基因组提取与测序拼接
采用CTAB法提取噬菌体DNA，具体步骤参考文献[17]。提取后的DNA通过琼脂糖凝胶电泳法检验无蛋白等杂质污染后，再进行16S rRNA基因PCR扩增检测，以确认无宿主污染，细菌引物(27F、1492R)和反应体系参考赵欣卓等[16]的方法。
噬菌体Ste-X和Ste-D的DNA由上海凌恩生物科技有限公司进行二代测序及拼接。全基因组序列已提交至国家微生物科学数据中心(National Microbiology Data Center, NMDC)，编号分别为NMDC60197967和NMDC60197966。
1.9 噬菌体基因组分析与基因功能注释
利用BLASTn (http://blast.ncbi.nlm.nih.gov/)对核苷酸序列相似性进行鉴定；用Easyfig 2.2.5绘制Ste-X和Ste-D的全基因组比对图。通过BLASTp (http://www.ncbi.nlm.nih.gov/)进一步校正预测注释蛋白的功能；使用tRNAscan-SE (http://lowelab.ucsc.edu/tRNAscan-SE/)搜索tRNA序列[18]；CARD数据库(https://card.mcmaster.ca/analyze/blast)用于识别抗生素耐药性基因；VFDB数据库(https://www.mgc.ac.cn/VFs/main.htm)用于鉴定基因组中潜在的毒力基因。使用MEGA 11.0软件对噬菌体的全基因组序列及保守序列编码的主要衣壳蛋白序列采用邻接法(neighbor-joining method)构建系统发育树。
1.10 噬菌体ORFs编码蛋白质的一级结构预测、结构域分析及二级、三级结构预测
利用Expasy-ProtParam (https://web.expasy.org/protparam/)预测蛋白质的基本理化性质；利用NCBI保守结构域数据库(https://www.ncbi.nlm.nih.gov/Structure/cdd/wrpsb.cgi)进行保守结构域分析；利用SOPMA (https://npsa-prabI.Ibcp.fr/cgI-bin/npsa_automat.pl?page=npsa%20_sopma.html)预测二级结构；使用SWISS-MODEL在线软件(https://swissmodel.expasy.org/)对蛋白质进行三维结构预测。
2 结果与分析
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2.1 噬菌体生物学特性
从校园人工湖水样中分离到2株能侵染S. indicatrix EB12的噬菌体Ste-X和Ste-D，Ste-X噬菌斑小且清晰透亮(图1A)，而Ste-D噬菌斑较大且有晕圈(图1C)。经电镜观察，2株噬菌体均为短尾噬菌体(图1B、1D)，Ste-X的头部直径为(61.700±0.972) nm (n=30)，尾长为(18.600±1.064) nm (n=30)；Ste-D的头部直径为(59.000±2.170) nm (n=30)，尾长为(9.800±0.621) nm (n=30)。
将噬菌体与宿主菌液分别按不同感染复数混合，采用双层平板法测定其效价(表1)。结果显示，噬菌体Ste-X和Ste-D达到最大效价时的最佳感染复数分别为1 000和10。
将噬菌体Ste-X和Ste-D分别按最佳感染复数与宿主菌混合后测定其效价并绘制一步生长曲线。2株噬菌体的潜伏期均为20 min，裂解期分别为60 min和70 min，裂解量分别为28.8 PFU/cell和131.1 PFU/cell (图1E)。将2株噬菌体置于30 W紫外灯下30 cm处照射，结果显示，噬菌体Ste-X在紫外照射60 min后完全失活，而Ste-D在紫外照射120 min后才完全失活(图1F)。在pH耐受性方面，噬菌体Ste-X在pH 5.0-9.0时活性最高，pH 3.0-4.0时效价显著降低甚至完全失活，而pH 11.0-13.0时虽然效价降低但仍保持部分活性；噬菌体Ste-D在pH 3.0-12.0时均能存活，仅在pH 13.0时完全失活(图1G)。在热稳定性方面，噬菌体Ste-X在20-40 ℃时效价较高，超过40 ℃后时效价随温度升高而降低，70 ℃时完全失活；噬菌体Ste-D在20-50 ℃时效价较高，超过50 ℃后效价随温度升高而降低，80 ℃时完全失活(图1H)。
2.2 噬菌体宿主范围
供试宿主菌株共10株，分别隶属于5个属，均分离自大庆湿地水体蓝藻附着细菌。除S. nematodicola和R. rosettiformans外，其余 8株细菌均对蓝藻有促生效果。噬菌体Ste-X和Ste-D仅能侵染除自身宿主外的1株P. sediminis，但噬菌斑并不清晰，侵染能力较弱(表2和图2A、2B)。
2.3 噬菌体Ste-X和Ste-D的基因组特征
噬菌体Ste-X和Ste-D的基因组均为环状DNA，2株噬菌体的全基因组序列相似度达到99.99%，其基因组特征基本相同。经ClustalW序列比对后发现，仅有3个碱基不同，分别位于23 219、23 220和34 748 bp处，涉及编码ORF34和ORF52。2株噬菌体的全长均为39 429 bp，Ste-X和Ste-D的G+C含量分别为57.80%和57.85% (图3A、3B)。2株噬菌体均仅预测到1个tRNA基因，位于36 231 bp与 36 159 bp之间，且未预测到毒力和耐药基因。二者均含有47个正向转录基因以及18个反向转录基因。
2.4 噬菌体Ste-X和Ste-D的功能注释
对2株噬菌体的基因组进行功能注释发现，噬菌体Ste-X和Ste-D的基因组均含有65个ORFs。通过NCBI NR进行在线注释后，均得到29个ORFs，占全部ORFs的44.62%，其中17个ORFs为假设蛋白，剩余12个编码的功能分为宿主裂解蛋白(3个)、结构蛋白(4个)、DNA包装蛋白(1个)和复制与调节蛋白(4个)，这些蛋白相互协作，共同完成噬菌体的整个侵染过程。
宿主裂解蛋白：ORF27编码果胶裂解酶超家族蛋白；ORF50编码穴蛋白，是一种可以实现跨膜运输使裂解酶到达细胞壁肽聚糖层进而裂解宿主的小分子膜蛋白[19]；ORF54假定溶菌酶，可编码破坏细菌细胞壁[20]。结构蛋白：ORF28编码病毒结构蛋白；ORF35编码尾管蛋白；ORF40编码假定主要衣壳蛋白；ORF44编码头尾连接蛋白。DNA包装蛋白：ORF48编码末端酶小亚基。复制与调节蛋白：ORF3编码类DnaB复制解旋酶；ORF16编码关键重组功能蛋白；ORF34编码部分稳定蛋白；ORF56是一种对DNA四向结构(holliday junctions, HJs)具有高度特异性的内切酶，可有效修复DNA并准确分离染色体，以维持基因组的稳定性[21]。
2.5 噬菌体Ste-X和Ste-D的系统进化分析
两株噬菌体经BLASTn比对结果显示有 6条噬菌体的全基因组序列与其相似度在92%以上，但覆盖度较低(0.09%-0.12%)。下载与噬菌体全基因组序列及保守序列编码的假设主要衣壳蛋白(ORF40)同源性较高的噬菌体的核苷酸序列，采用邻接法构建基因组系统发育树(图4A、4B)结果显示，与噬菌体Ste-X和Ste-D亲缘关系最近的噬菌体分别是Ralstonia phage Firinga (NC_054961)和Ralstonia phage RSK1 DNA (AB863625)，覆盖度为0.12%，均属于有尾噬菌体目；主要衣壳蛋白构建的系统发育树结果显示，与2株噬菌体亲缘关系最近的噬菌体也是2株有尾噬菌体(UOF83055、DAQ54372)，覆盖率分别为100%和98%，相似度分别为50.00%和46.98%；将2株噬菌体与其亲缘关系最近的噬菌体的基因组进行共线性比较(图5)，噬菌体Ste-X和Ste-D与其亲缘关系最近的2株噬菌体长度基本相同，噬菌体Ste-X和Ste-D二者整体基因排布无差别，但与另外2株噬菌体的差异较大。基于上述结果，认为噬菌体Ste-X和Ste-D可能为新型有尾噬菌体。
2.6 两株噬菌体ORF34和ORF52编码蛋白质的一级结构预测及结构域分析
将2株噬菌体基因组中3个不同碱基所在的ORFs进行结构预测，采用Expasy-ProtParam软件分析发现，2株噬菌体ORF34所编码的蛋白质氨基酸数量均为865个，相对分子质量分别为93 831 Da和93 846 Da，等电点均小于7，均为酸性蛋白质。通过比较氨基酸组成成分发现，噬菌体Ste-X的Leu和Lys数量分别为58个和19个，而Ste-D的Leu和Lys数量分别为59个和18个，其余氨基酸组成成分相同。噬菌体Ste-X和Ste-D所编码的蛋白质所带负电荷氨基酸残基数量均为88个，正电荷氨基酸残基数量分别为66个和65个。2种蛋白质的不稳定系数均小于40，脂肪系数分别为78.13和77.68，说明其稳定性较好。总平均亲水性为负值(图6A、6B)，大部分氨基酸得分均小于0，因此2株噬菌体中ORF34编码的蛋白质均为稳定的亲水酸性蛋白。
两株噬菌体ORF52所编码的蛋白质氨基酸数量均为130个，相对分子质量分别为14 098 Da和14 156 Da，等电点均大于7，均为碱性蛋白质。通过比较氨基酸组成成分发现，噬菌体Ste-X的Asp和Gly数量分别为7个和12个，而Ste-D的Asp和Gly数量分别为6个和13个，其余氨基酸组成成分相同。2种蛋白质所带正电荷氨基酸残基数量均为17个，负电荷氨基酸残基数量分别为16个和15个。脂肪系数均为66.92，不稳定系数分别为42.84和42.91，均大于40.00，说明其稳定性较差。总平均亲水性为负值(图6C、6D)，大部分氨基酸得分均小于0，因此，2种噬菌体中ORF52编码的蛋白质均为稳定性差的亲水碱性蛋白。
利用NCBI保守结构域数据库(Conserved Domains)分析氨基酸序列的保守结构域，结果显示，2株噬菌体的ORF34所编码的蛋白质均含有ChtBD3和PHA00661超家族，分别位于106- 144和5-862氨基酸残基处。ChtBD3超家族包含与几丁质酶及相关酶的结合域，编码的蛋白质可以破坏革兰氏阴性细菌的细胞壁[22]；PHA00661超家族为假设蛋白；ORF52编码的蛋白质则未检测到保守结构域。
2.7 两株噬菌体ORF34和ORF52编码蛋白质的二级结构及三级结构预测
利用SOPMA软件分析二级结构(图7A)，结果显示2株噬菌体ORF34编码的蛋白质均以无规则卷曲结构为主，分别占64.51% (Ste-X)和63.58% (Ste-D)；其次为延伸链，分别占25.43% (Ste-X)和26.94% (Ste-D)；α螺旋占比最低，分别为10.06% (Ste-X)和9.48% (Ste-D)。ORF52编码的蛋白质以α螺旋为主，占比51.54%；其次为无规则卷曲，分别占31.00% (Ste-X)和31.54% (Ste-D)；延伸链占比最低，分别为18.46% (Ste-X)和16.92% (Ste-D)。
利用Swiss-Model在线软件对蛋白质的三维结构进行同源建模(图7B、7C)，结果显示三级结构模型预测结果与二级结构一致。2株噬菌体ORF34所编码的主要蛋白空间结构均为无规则卷曲；ORF52编码的蛋白空间结构相同，主要为α螺旋。2株噬菌体仅在第547个氨基酸存在差异，但编码蛋白质的空间结构仍为无规则卷曲。
3 讨论与结论
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寡养单胞菌，也称为窄食单胞菌，最早被发现的菌株是嗜麦芽寡养单胞菌(S. maltophilia)，且早期发现的该菌多为植物内生菌[1]。近年来，S. maltophilia作为条件致病菌，易引发败血症、心内膜炎及尿路感染等病症，受到广泛关注，该病原菌的多重耐药性促使临床上对其耐药机制[23]和噬菌体疗法的使用进行深入研究[24]。自1993年寡养单胞菌属建立以来，环境中分离获得菌株从生理生化特性、细胞化学成分和分子生物学特征等多角度不断完善其系统分类，直至2018年，S. indicatrix才形成独立分支[25]，其全基因组序列于2021年首次报道[26]。S. indicatrix广泛存在于向日葵[27]、土壤[28]、蔬菜[29]和天然水体[26]中，能够减轻植株的环境胁迫。近期研究发现，一株寡养单胞菌(Stenotrophomonas sp.)莱茵衣藻(Chlamydomonas reinhardtii) P3培养过程中，可削弱高浓度甲酸对藻类的抑制作用，从而促进其生长[29]。此外，Bertolini等[30]等于2014年首次从高硒豆科植物黄芪根际分离出一株S. indicatrix，该菌株对亚硒酸盐具有高耐受性并可将其还原为元素硒供植物生长；向日葵根际分离的S. indicatrix (2018年之前被归为S. maltophilia)也与植物生长调控和病原菌抑制相关[31]。本实验室分离的S. indicatrix EB12来自蓝藻附生细菌，对蓝藻生长具有促生作用。若采用S. indicatrix噬菌体裂解其宿主细胞，有望调控水体中蓝藻的生长。
噬菌体的生物学特性研究可为探索噬菌体生长环境条件及调控宿主种群提供理论基础。然而，关于S. indicatrix噬菌体的生物学特性尚未见报道[1]，而寡养单胞菌属其他菌株的噬菌体研究则较多。噬菌体的潜伏期及裂解量是衡量其裂解能力的重要指标。S. maltophilia噬菌体的潜伏期为5-75 min[12-13]，裂解量为43.2-3 000 PFU/cell[32-33]。本研究中2株侵染S. indicatrix的噬菌体Ste-X和Ste-D的潜伏期均为20 min，裂解量分别为28.8 PFU/cell和131.1 PFU/cell，均为烈性短尾噬菌体。噬菌体Ste-X和Ste-D的最佳感染复数分别为1 000和10，与已报道的S. maltophilia噬菌体[32]存在较大差异。噬菌体Ste-X和Ste-D的pH耐受范围分别为pH 4.0-13.0和pH 3.0-12.0，较侵染S. maltophilia的噬菌体YCR3A-1[32]的pH耐受范围(pH 5.0-11.0)更广。噬菌体Ste-X在超过40 ℃时活性开始下降，70 ℃时失活，而噬菌体Ste-D在70 ℃高温下仍具有活性，这与侵染S. maltophilia的噬菌体BUCT609[34]相似，均表现出一定的耐高温能力。蛋白质和核酸吸收紫外线后作用于DNA并使其结构遭到破坏，从而导致DNA丧失转化能力，使噬菌体失去活性[35]。噬菌体Ste-X和Ste-D分别在紫外照射60 min和120 min后才完全失活，表现出一定的耐紫外能力。噬菌体Ste-X和Ste-D的宿主范围较窄，具有专一性，除自身宿主外，仅能侵染1株P. sediminis，且噬菌斑不明显，侵染能力较弱。寡养单胞菌噬菌体的形态多样，包括肌尾[13,36]、短尾[34]、长尾[12,32]和丝状[37]等。从电镜照片来看，噬菌体Ste-X和Ste-D均属于有尾噬菌体目、短尾噬菌体科。
目前已分离的寡养单胞菌噬菌体全基因组序列长度在6 867 bp-250 kb[37-38]之间，噬菌体Ste-X和Ste-D的基因组长度均为39 429 bp，二者全基因组序列高度相似达99.99%，仅存在 3个碱基差异，分别位于23 219、23 220和 36 429 bp处，涉及ORF34和ORF52的编码。这3个碱基的差异导致2株侵染S. indicatrix的噬菌体(Ste-X和Ste-D)在生物学特性(裂解量、最佳感染复数、温度、pH和紫外线耐受性)方面存在显著差异。基因组结构决定了噬菌体的功能，因此，本研究对2个差异ORFs编码蛋白的一级、二级和三级结构进行了比较分析。ORF34编码的蛋白质具有保守结构域，是一种稳定的亲水酸性蛋白，其功能可能与破坏革兰氏阴性细菌细胞壁[22]相关，进而影响裂解量和最佳感染复数，但具体机制尚需进一步实验验证。Pan等[39]发现，Hafnia噬菌体在传代过程中形成的噬菌斑大小不同，高通量测序结果显示，较小的噬菌斑与正常噬菌斑相比缺失了一段HNH归巢内切酶(HEG)基因，研究表明单个基因片段的缺失或单个碱基突变均会导致噬菌体形态及功能的变化。Guo等[15]通过紫外诱变的方式证明，单个碱基突变会导致噬菌体的pH耐受范围、噬菌斑形态和侵染能力的改变，这与本研究结果相似。除噬菌斑形态及侵染能力外，本研究的 2株噬菌体在紫外线耐受能力方面也存在较大差异。光损伤现象主要由环丁烷嘧啶二聚体(cyclobutane pyrimidine dimer, CPDs)和嘧啶(6-4)嘧啶酮[pyrimidine (6-4) pyrimidone, 简称(6-4)光产物] 2种类型的嘧啶二聚体产物阻碍了DNA的复制及转录[40]。生物可通过紫外光修复系统对受损DNA进行修复，而紫外线修复系统广泛存在于水生微生物及噬菌体中[41]。噬菌体中DNA紫外光修复系统的相关基因是决定噬菌体耐紫外能力强弱的关键因素。本研究的2株噬菌体除ORF34和ORF52外，其余基因模块组成均相同，但在噬菌斑形态及耐紫外光能力等方面差异较大。推测这2个基因模块可能与噬菌体的紫外光修复能力有关，具体功能有待进一步实验验证。
噬菌体是地球上数量最大的生物实体(约有1031个)[14]，能够高效且特异性地识别并杀灭宿主细菌，在医疗、农业及环境保护等领域具有广阔的应用前景。本研究从水体蓝藻的附生细菌中分离到的S. indicatrix对藻类具有促生效果，其噬菌体可能通过影响S. indicatrix的数量及活性，进而间接调控水体中蓝藻的生长。通过对 2株噬菌体生物学特性的调查和基因组分析，发现仅存在3个差异碱基的2株侵染S. indicatrix的短尾噬菌体在全基因组水平上表现出显著的生物学特性差异。本研究为深入探索S. indicatrix与其噬菌体的相互关系提供了基础资料。
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  • 国家重点研发计划(2022YFD1500202)
  • 国家自然科学基金(31870477)
  • 黑龙江省自然科学基金(C2017045)
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doi: 10.13343/j.cnki.wsxb.20240833
  • 接收时间：2024-12-20
  • 首发时间：2026-02-06
  • 出版时间：2025-07-04
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  • 收稿日期：2024-12-20
  • 录用日期：2025-01-07
基金
National Key Research and Development Program of China(2022YFD1500202)
国家重点研发计划(2022YFD1500202)
National Natural Science Foundation of China(31870477)
国家自然科学基金(31870477)
Natural Science Foundation of Heilongjiang Province(C2017045)
黑龙江省自然科学基金(C2017045)
作者信息
    1.黑龙江八一农垦大学 生命科学技术学院，黑龙江省寒区环境微生物与农业废弃物资源化利用重点实验室，黑龙江 大庆
    2.中国科学院东北地理与农业生态研究所，黑土区农业生态重点实验室，黑龙江 哈尔滨
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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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