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2022 , Vol. 43 >Issue 3: 455 - 462

DOI: https://doi.org/10.3969/j.issn.1000-2561.2022.03.003

Omics ＆ Biotechnology

Analysis of Complete Genome Sequence of Streptomyces solisilvae HNM0141Tof the Streptomyces violaceusniger Clade

  • ZHOU Yifan 1, 2 ,
  • LI Chengui 1 ,
  • XU Yun 1 ,
  • WU Wenqiang 1 ,
  • XIA Wei 2 ,
  • HUANG Xiaolong 1 ,
  • HUANG Dongyi 2 ,
  • ZHOU Shuangqing , 1, 3, *
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  • 1. Key Laboratory of Tropical Biological Resources of Ministry of Education, Haikou, Hainan 570228, China
  • 2. College of Tropical Crops, Hainan University, Haikou, Hainan 570228, China
  • 3. Pharmacy School of Guilin Medical University, Guilin, Guangxi 541199, China
*ZHOU Shuangqing,E-mail：

Received date: 2021-05-10

  Request revised date: 2021-06-16

  Online published: 2022-03-23

Copyright

Copyright reserved © 2022. Office of Acta Agronomica Sinica All articles published represent the opinions of the authors, and do not reflect the official policy of the Chinese Medical Association or the Editorial Board, unless this is clearly specified.
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Abstract

Actinomycetes belonging to Streptomyces are the most important antibiotic producing bacteria and also the actinomycete genus with the largest number of species. Many streptomycete type strains can be assigned to distinct evolutionary clades on the 16S rRNA gene phylogenetic tree, and the S. violaceusniger 16S rRNA gene clade is one of them. Members of the clade form a greyish yellow substrate mycelium and a grayish aerial hyphae on oatmeal agar that develop into spiral chains of rugose ornamented spores that become black on prolonged incubation. Members of the S. violaceusniger 16S rRNA gene clade have abundant biological activities and produce antibacterial metabolites, antiparasitic metabolites, antitumour compounds and immunosuppressants as important sources for the development and utilization of new antibiotics. S. solisilvae HNM0141Tis a type strain assigned to the S. violaceusniger 16S rRNA gene clade. Here, we present the complete genome sequence of it, which is generated using the third sequencing technology and consists of a linear chromosome of 11 639 536 bp with a GC content of 71.3%, 9363 protein coding genes(CDS), 18 rRNA genes, and 67 tRNA genes. The identified CDS were classified into 6376, 5886, and 3246 categories based on clusters of orthologous genes of proteins (COG), gene ontology (GO), and Kyoto Encyclopedia of Genes and Genomes (KEGG) designation, respectively. In addition to the general function prediction only, most of the genes involved in transcription, amino acid transport and metabolism, carbohydrate transport and metabolism and secondary metabolic biosynthesis and metabolism were accounted for 12.91%,10.25%, 8.89% and 7.59% respectively. Forty-eight putative secondary metabolite biosynthetic gene clusters were found in the genome using the online antiSMASH software, including eight PKS, seven NRPS, fourteen hybrid gene clusters, six terpenes, three siderophores, two butyrolactones, one NAPAA, one ectoine, one lanthipeptide-class-i, one ladderane, one indole, one RiPP-like, one hserlactone and one redox-cofactor. Polyketone (PKS) and non-ribosomal peptide (NRPS) gene clusters (including heterozygous types) were abundant and accounted for more than 50% of the total gene clusters. Seven putative gene clusters showed 100% similarities to known gene clusters: pristinol, ectoine, geosmin, desferrioxamin B, echoside A/B/C/D/E, nigericin, and coelichelin gene clusters. Thirty-four putative gene clusters showed 2%-96% similarities to known gene clusters. The remaining seven gene clusters could not be matched to known gene clusters. Genome-wide analysis showed that S. solisilvae HNM0141T had strong ability of the biosynthesis of secondary metabolites, indicated that it should be good research potential for mining of the novel antibiotics.

Key words： Streptomyces violaceusniger; 16S rRNA gene clade; genome sequence; secondary metabolite biosynthetic gene clusters

Cite this article

ZHOU Yifan , LI Chengui , XU Yun , WU Wenqiang , XIA Wei , HUANG Xiaolong , HUANG Dongyi , ZHOU Shuangqing . Analysis of Complete Genome Sequence of Streptomyces solisilvae HNM0141Tof the Streptomyces violaceusniger Clade[J]. Chinese Journal of Tropical Crops, 2022 , 43(3) : 455 -462 . DOI: 10.3969/j.issn.1000-2561.2022.03.003

链霉菌属是放线菌门种类最多的放线菌属,是最重要的抗生素产生菌。当前该属含有效发表种677个（ http://www.bacterio.net/streptomyces.html）。链霉菌属的有效发表种的模式菌株在16S rRNA基因序列系统发育树上分散归簇于不同的进化分枝（clade）[1],处在同一进化分枝上的菌株亲缘关系较近,通常表现出某些共同的生理特征。紫黑链霉菌16S rRNA基因进化枝（Streptomyces violaceusniger 16S rRNA gene clade）是其中的一个分枝（clade）,由SEMBIRING等[2]推荐建立。该分枝菌株在ISP3培养基上具有明显的特征：基内菌丝淡黄色,孢子丝早期灰色,后期黑褐色,孢子链呈螺旋状,表面不光滑,有褶皱[1,2]。利用特异性引物可以扩增到该分枝菌株16S rRNA基因序列中的部分特异性片段[3]。目前,该分枝包含正式发表的有效种共17个[4,5],在这些报道的有效种菌株中,许多菌株已经是知名的抗生素产生菌,如S. hygroscopicus和S. rapamycinicus。该分枝中的菌株普遍具有丰富的生物活性,能产生抗菌、抗虫、抗肿瘤、免疫抑制等多种活性物质,在抗生素的开发上得到了广泛的利用[4, 6]。因此,紫黑链霉菌16S rRNA基因进化枝菌株被认为是链霉菌属中利用价值极高的一类放线菌资源,是寻找新型抗生素的重要菌源。
研究发现该类菌在植物根际、非根际土壤、落叶堆、淡水沉积物、海洋沉积物等环境均具有分布,菌种的分布与环境具有相关性,特殊的环境蕴藏新颖的菌株[3]。也有研究者从植物的种子、叶鞘等内生环境分离到该分枝的菌株[7,8]。本实验室前期研究证实,紫黑链霉菌16S rRNA基因进化枝菌株在我国热带地区也有分布,不仅从海南药用植物根际分离到此类放线菌[9,10],也从热带雨林森林土壤中分离到此类放线菌的新种Streptomyces solisilvae HNM0141T[4]。为了深入地了解该分枝新种菌株HNM0141的生物学功能和次生代谢合成潜力,本研究采用Pacific BioscienceRS II系统上的SMRT对其进行全基因组测序,获得了菌株HNM0141的基因组全序列,同时进行了基因预测、功能注释与次级代谢合成基因簇分析,为该菌株的进一步研究和开发利用奠定基础。

1 材料与方法

1.1 材料

菌株Streptomyces solisilvae HNM0141T由实验室前期分离于海南霸王岭热带雨林土壤,保存于本实验室-20℃冰箱甘油管中。

1.2 方法

1.2.1 菌株HNM0141 DNA的提取与基因组测序 菌株HNM0141使用ISP2液体培养基28℃,摇瓶培养5 d,离心收集菌体,使用Promega（美国）Wizard®基因组DNA提取试剂盒进行总DNA的提取。送北京百迈客科技有限公司,利用Pacific BioscienceRS II系统上的SMRT进行全基因组测序。获得的数据用HGAP 2.3软件[11]进行拼接组装获得基因组完全图,采用Circos version 0.62软件[12]绘制基因组圈图。
1.2.2 基因预测、功能注释与次级代谢合成基因簇分析 将拼接好的基因组序列采用Glimmer 3.02软件[13]预测其开放阅读框（ORF）;使用tRNAscan-SE[14]软件预测tRNA,采用软件Infernal 1.1[15]基于Rfam[16]数据库预测基因组中的rRNA以及除了tRNA和rRNA之外的其他ncRNA。将所有的ORF预测的蛋白序列采用BLAST软件完成比对及功能注释。CDS和Genes的功能注释分别采用COG（Clusters of orthologous groups）、GO（Gene ontology）和KEGG（Kyoto encyclopedia of genes and genomes）数据库完成。采用antiSMASH 6.0（ http://antismash.secondarymetabolites.org）在线软件预测菌株HNM0141的次级代谢生物合成基因簇。
1.2.3 基因组系统发育树构建 将获得的菌株HNM0141的基因组序列,利用Type Strain Genome Server（ https://tygs.dsmz.de/）在线软件构建基因组水平的系统发育树,从基因组水平判断菌株的系统发育地位。

2 结果与分析

2.1 基因组的组装与功能注释

菌株HNM0141经测序、组装获得完整的基因组,长度为11 639 536 bp,GC含量71.03%的线形染色体（GenBank登录号：CP065050）。基因组预测获得总共9363个蛋白编码基因,18个rRNA,67个tRNA基因和193 ncRNA基因（图1和表1）。其中,9363个CDS（蛋白质编码序列）中有6376、5886、3246个CDS分别在COG、GO和KEGG数据库中得到功能注释。
图1 菌株S. solisilvae HNM0141T全基因组染色体圈图

最外面一圈为基因组大小的标示,每个刻度为0.1 Mb;第二圈和第三圈分别为基因组正链和负链的基因,不同颜色代表不同的COG功能分类;第四圈为重复序列;第五圈为tRNA 和rRNA;第六圈为GC含量,浅黄色部分表示该区域GC含量高于基因组的平均GC含量,蓝色部分则表示该区域GC含量低于基因组的平均GC含量;最内圈是GC-skew,深灰色代表G含量大于C的区域,红色代表C含量大于G的区域。

Fig. 1 Circular representation of the strain of S. solisilvae HNM0141T

The outermost circle is the mark of genome size, with each scale of 0.1 MB; The second and third circles are the positive and negative genes of genome respectively, Different colors represent different COG functional classification; The fourth circle is repetitive sequence; The fifth circle is tRNA and rRNA genes; The sixth circle is the GC percentage plot, pale yellow above average, blue below average; The innermost layer is the GC skew, dark gray represents areas with more G than C, and red represents areas with more C than G.

表1 菌株S. solisilvae HNM0141T的基因组特性

Tab. 1 Genome features of S. solisilvae HNM0141T

特征Feature 染色体特征Chromosome characteristic
基因组拓扑结构 线性
染色体大小/bp 11 639 536
GC含量/% 71.03
蛋白质编码基因 9363
基因平均长度/bp 1095
COG注释基因 6376
KEGG注释基因 3246
GO注释基因 5886
rRNA基因 18
tRNA基因 67
ncRNA基因 193
假基因 11

2.2 COG功能分类

在6376个CDS具有COG功能注释中,共分为25个功能组（图2）。其中,除了一般功能预测（R）之外,有大部分基因参与转录（K）、氨基酸转运和代谢（E）、碳水化合物转运和代谢（G）以及次级代谢生物合成和代谢（Q）,基因数占比分别为12.91%、10.25%、8.89%和7.59%。同时在生物代谢大类中,包括能量产生和转化（C）（6.41%）、氨基酸转运和代谢（E）（10.25%）、核苷酸转运和代谢（F）（1.27%）、碳水化合物转运和代谢（G）（8.89%）、同工酶转运和代谢（H）（3.32%）、脂质转运和代谢（I）（5.51%）、无机离子转运和代谢（P）（5.6%）、次级代谢生物合成和代谢（Q）（7.59%）、信号传导与代谢（T）（4.97%）以及防御代谢（V）（1.6%）,这些基因占所有功能基因的55.41%。由此可见,菌株HNM0141有相当强的生物代谢能力,特别在次级代谢生物合成方面可能具有强大的合成能力。
图2 菌株S. solisilvae HNM0141T的COG同源基因注释分类

Fig. 2 COG homologous gene annotation classification of S. solisilvae HNM0141T

2.3 GO功能分类

5886个CDS具有GO注释功能,共分为3大类: 细胞组分（cellular component）、分子功能（molecular function）和生物学过程（biological process）（图3）。分子功能中的催化活性和结合,生物学过程中的代谢过程、细胞过程、单生物过程和生物调节等相关基因数量最多。
图3 菌株S. solisilvae HNM0141T的GO功能聚类分析

Fig. 3 GO functional cluster analysis of S. solisilvae HNM0141T

2.4 菌株HNM0141的基因组系统发育分析

将菌株HNM0141的基因组完成序列,利用Type Strain Genome Server在线软件,构建基因组水平的系统发育树如图4所示,菌株HNM0141与链霉菌属的菌株聚类在一起,特别跟标准菌株S. rapamycinicus,S. violaceusniger,S. melanosporofaciens,S. antimycoticus,S. sporoclivatus,S. sporocinereus和S. himastatinicus聚合在同一个大的分枝上,而这些标准菌株都为紫黑链霉菌16S rRNA 基因进化枝（Streptomyces violaceusniger 16S rRNA gene clade）的主要成员[2]。因此,从基因组水平的系统发育树再次证明了菌株HNM0141为紫黑链霉菌16S rRNA基因进化枝的新种菌株[4]。
图4 菌株HNM0141的基因组系统发育树

Fig. 4 Phylogenomic tree of strain HNM0141

2.5 次级代谢合成基因簇分析

在菌株S. solisilvae HNM0141T基因组预测到48个次级代谢产物合成基因簇（表2）,其类型包括8个聚酮（PKS）型、7个非核糖体肽（NRPS）型（2个NRPS-like）、14个杂合型、6个terpene、3个siderophore、2个butyrolactone,其余NAPAA、ectoine、lanthipeptide-class-i、ladderane、indole、RiPP-like、hserlactone、redox-cofactor各1个。其中包含PKS型和NRPS型（包括杂合类型）的基因簇占总基因簇的50%以上。从基因簇的相似性来看,有7个基因簇（Cluster10、Cluster17、Cluster24、Cluster25、Cluster26、Cluster39、Cluster44）与已知基因簇的相似性为100%,说明菌株S. solisilvae HNM0141具有产生代谢物pristinol、ectoine、geosmin、desferrioxamin B、echoside A/B/C/D/E、nigericin、coelichelin的能力。7个基因簇（Cluster16、Cluster18、Cluster19、Cluster27、Cluster29、Cluster34、Cluster35）无法匹配到已知基因簇,表明这些基因簇为未知基因簇,具有产生新代谢物的潜能。其他34个基因簇的相似性在2%~96%之间,暗示这些基因簇具有产生已知结构代谢物或其结构类似物的潜力。
表2 菌株S. solisilvae HNM0141T基因组中预测的生物合成基因簇

Tab. 2 Predicted biosynthesis clusters in S. solisilvae HNM0141T

编号
Number		 基因簇类型
Gene cluster type		 起始
Start		 终止
End		 可能的代谢物
Possible metabolite		 相似性
Similarity
Cluster1 T3PKS,T1PKS,nucleoside 86 666 290 037 herboxidiene 17%
Cluster2 NAPAA 509 374 543 540 nocathiacin 4%
Cluster3 NRPS-like 823 523 861 942 echoside A 11%
Cluster4 lanthipeptide-class-ii,NRPS,T1PKS 901 188 975 916 meilingmycin 3%
Cluster5 terpene 1 084 443 1 105 416 brasilicardin A 38%
Cluster6 NRPS 1 131 305 1 208 557 herboxidiene 4%
Cluster7 RiPP-like,T1PKS,hglE-KS 1 220 124 1 354 311 pentamycin 40%
Cluster8 T1PKS,NRPS-like 1 486 754 1 569 652 hygrocin A/B 96%
Cluster9 T1PKS,NRPS 1 574 460 1 691 041 meridamycin 60%
Cluster10 terpene 1 888 573 1 908 108 pristinol 100%
Cluster11 betalactone,T1PKS,NRPS-like 1 995 673 2 092 181 geldanamycin 73%
Cluster12 terpene,PKS-like 2 411 004 2 454 761 rustmicin 23%
Cluster13 T1PKS,NRPS-like 2 529 900 2 605 586 JBIR-100 55%
Cluster14 T1PKS,NRPS-like 2 644 207 2 723 750 hygrocin A 38%
Cluster15 terpene 2 914 424 2 931 169 BE-43547A1 20%
Cluster16 siderophore 2 984 440 2 996 564
Cluster17 ectoine 3 161 992 3 172 396 ectoine 100%
Cluster18 terpene 3 668 551 3 689 528
Cluster19 lanthipeptide-class-i 3 867 776 3 894 241
Cluster20 T1PKS 4 298 355 4 480 568 mediomycin A 65%
Cluster21 ladderane 4 646 473 4 687 134 atratumycin 28%
Cluster22 NRPS 4 737 269 4 779 394 CDA1b / CDA2a 5%
Cluster23 indole 4 983 765 5 004 913 5-isoprenylindole-3-carboxylate β-D-glycosyl ester 61%
Cluster24 terpene 5 592 064 5 613 426 geosmin 100%
Cluster25 siderophore 6 686 017 6 697 095 desferrioxamin B 100%
Cluster26 NRPS-like 7 232 398 7 272 380 echoside A/B/C/D/E 100%
Cluster27 siderophore 7 827 940 7 839 748
Cluster28 ladderane,arylpolyene,NRPS 7 923 088 8 009 996 atratumycin 57%
Cluster29 RiPP-like 8 116 046 8 127 566
Cluster30 T1PKS 8 187 954 8 248 591 s56-p1 11%
Cluster31 T2PKS 8 360 569 8 433 084 spore pigment 83%
Cluster32 terpene 8 616 532 8 643 063 hopene 76%
Cluster33 NRPS,betalactone 8 871 344 8 996 389 malacidin A / malacidin B 28%
Cluster34 T1PKS 9 087 895 9 135 563
Cluster35 butyrolactone 9 307 117 9 316 675
Cluster36 hserlactone 9 328 723 9 349 481 daptomycin 3%
Cluster37 redox-cofactor 9 462 583 9 484 674 lankacidin C 13%
Cluster38 T1PKS 9 515 969 9 591 470 elaiophylin 87%
Cluster39 T1PKS 9 725 085 9 855 977 nigericin 100%
Cluster40 T1PKS 10 072 562 10 210 083 azalomycin F3a 91%
Cluster41 NRPS 10 236 552 10 323 205 glycinocin A 53%
Cluster42 butyrolactone 10 355 073 10 366 068 cyphomycin 9%
Cluster43 T3PKS,T1PKS,betalactone,NRPS 10 482 177 10 607 314 totopotensamide A / B 64%
Cluster44 NRPS 10 625 337 10 675 669 coelichelin 100%
Cluster45 NRPS,ladderane,arylpolyene 10 908 112 10 980 633 RP-1776 20%
Cluster46 T1PKS 11 037 304 11 082 029 leinamycin 2%
Cluster47 T1PKS,NRPS 11 165 594 11 275 146 rapamycin 28%
Cluster48 NRPS 11 574 300 11 627 584 ishigamide 11%

3 讨论

紫黑链霉菌16S rRNA基因进化枝放线菌以产生丰富的活性物质而著称。例如: S.rapamycinicus产生著名的免疫抑制剂雷帕霉素（rapamycin）[17];S. geldanamycininus产生格尔德霉素（geldanamycin）[1]以及S. malaysiensis产生阿扎霉素（azalomycin）[18];而吸水链霉菌S. hygroscopicus则是产生抗生素最多的放线菌,该类菌株能产生包括井冈霉素（validamycin）、米尔贝霉素（milbemycin）、双丙氨膦（bialaphos）、除莠霉素（herbimycin）等在内的650多种活性物质[19,20]。近年来,从一些特殊生境分离的紫黑链霉菌16S rRNA基因进化分枝菌株中发现了多种新颖的活性化合物。洪葵课题组从红树林来源的该分枝菌株211726中发现了7个具有强抗真菌和肿瘤活性的新型阿扎霉素F类大环内酯化合物[21];甘茂罗课题组从大连海洋沉积物来源的该分枝菌株7-145中挖掘到2个新型洋橄榄叶素（elaiophylin）和4个新型尼菲霉素（niphimycin）类化合物,对耐药菌MRSA和VRE呈现出较强的抗菌活性[22,23]。本实验室从S. solisilvae HNM30702中分离到阿扎霉素Azalomycin F4a和F5a,以及具抗病毒活性的新颖环六肽Soliseptide A[24]。基因组测序显示该分枝放线菌菌株的基因组普遍大于一般的链霉菌,如S. hygroscopicus 5008基因组长度为10.3 Mb[25],S. rapamycinicus NRRL 5491的基因组长度为12.7 Mb[17],S. hygroscopicus subsp. hygroscopicus NBRC 16556基因组长度为10.1 Mb[26]。基因组学分析表明该分枝的菌株基因组中含有丰富的次级代谢产物合成基因簇,特别是聚酮类（PKS）和非核糖体肽（NRPS）类基因簇[17]。因此,对该类菌株进行全基因组测序分析将有助于从分子水平上了解其生物学功能和次级代谢产物的生物合成潜力,为深入开发与利用此类菌株提供理论依据。
本研究利用第三代全基因组测序技术,首次获得了模式菌株S. solisilvae HNM0141T的基因组完成图,其线状基因组长度大于11.6 Mb,符合该类菌株的基因组较大的基本特征。利用antiSMASH软件,预测得到48个次级代谢产物合成基因簇,且含有丰富的聚酮类（PKS）和非核糖体肽（NRPS）类（包括杂合类型）的基因簇,无疑证明了该菌株具有强大次级代谢产物合成的能力。同时发现该菌株基因组中含有与梅岭霉素（meilingmycin）、格尔德霉素（geldanamycin）、达托霉素（daptomycin）、阿扎霉素（azalomycin）、雷帕霉素（rapamycin）等知名抗生素合成基因簇相似性较低的基因簇（如：Cluster4、Cluster11、Cluster36、Cluster40、Cluster47）以及7个未知类型的基因簇,预示该菌株在新颖抗生素的挖掘上具有良好的开发潜能。

References

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