Diversity of Culturable Thermophilic Actinobacteria in Hot Springs in Tengchong, China and Studies of their Biosynthetic Gene Profiles

Microbial Ecology

Volumn 72, Issue 1, 2016, Pages 150-162

  Liu, Lan ^a   Salam, Nimaichand ^a   Jiao, Jian Yu ^b,c   Jiang, Hong Chen ^d   Zhou, En Min ^a,b   Yin, Yi Rui ^b   Ming, Hong ^b,e   Li, Wen Jun ^a,b  

^a SUN YAT SEN UNIVERSITY   (China)

^b YUNNAN UNIVERSITY   (China)

^c KUNMING UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

^d CHINA UNIVERSITY OF GEOSCIENCES   (China)

^e XINXIANG MEDICAL UNIVERSITY   (China)

Author keywords

16S rRNA gene; Antimicrobial activity; PKS and NRPS genes; Tengchong hot springs; Thermophilic actinobacteria

Indexed keywords

BACTERIAL DNA; RNA 16S;

ACTINOBACTERIA; BIODIVERSITY; CHINA; CLASSIFICATION; DNA SEQUENCE; GENETICS; HEAT; ISOLATION AND PURIFICATION; MICROBIOLOGY; PHYLOGENY; THERMAL SPRING;

ACTINOBACTERIA; BIODIVERSITY; CHINA; DNA, BACTERIAL; HOT SPRINGS; HOT TEMPERATURE; PHYLOGENY; RNA, RIBOSOMAL, 16S; SEQUENCE ANALYSIS, DNA;

EID: 84962779572     PISSN: 00953628     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00248-016-0756-2     Document Type: Article

References (57)

1. Alain K, Querellou J (2009) Cultivating the uncultured: limits, advances and future challenges. Extremophiles 13:583–594
2. Amann R (2000) Who is out there? Microbial aspects of biodiversity. Syst Appl Microbiol 23:1–8
3. Amos GCA, Borsetto C, Laskaris P, Krsek M, Berry AE, Newsham KK, Calvo-Bado L, Pearce DA, Vallin C, Wellington EMH (2015) Designing and implementing an assay for the detection of rare and divergent NRPS and PKS clones in European, Antarctic and Cuban soils. PLoS ONE 10:e0138327. doi:10.1371/journal.pone.0138327
4. Ayuso-Sacido A, Genilloud O (2005) New PCR primers for the screening of NRPS and PKS-I systems in Actinomycetes: detection and distribution of these biosynthetic gene sequences in major taxonomic groups. Microb Ecol 49:10–24
5. Becerril-Espinosa A, Freel KC, Jensen PR, Soria-Mercado IE (2013) Marine actinobacteria from the gulf of California: diversity, abundance and secondary metabolite biosynthetic potential. Antonie Van Leeuwenhoek 103:809–819
6. Bentley SD, Chater KF, Ceerdeno-Tarraga GL, Thomson NR, James KD, Harris DE, Quail MA, Kieser H, Harper D, Bateman A, Brown S, Chandra G, Chen CW, Collins M, Cronin A, Fraser A, Goble A, Hidalgo J, Hornsby T, Howarth S, Huang CH, Kieser T, Larke L, Murphy L, Oliver K, O’Neil S, Rabbinowitsch E, Rajandream MA, Rutherford K, Rutter S, Seeger K, Saunders D, Sharp S, Squares R, Squares S, Taylor K, Warren T, Wietzorrek A, Woodward J, Barrel BG, Parkhill J, Hopwood DA (2002) Complete genome sequence of the model actinomycete Streptomyces coelicolor A3(2). Nature 417:141–147
7. Bérdy J (2005) Bioactive microbial metabolites. J Antibiot 58:1–26
8. Bérdy J (2012) Thoughts and facts about antibiotics: where we are now and where we are heading. J Antibiot 65:385–395
9. Bull AT (2011) Actinobacteria of the extremobiosphere. In: Horikoshi K (ed) Extremophiles handbook. Springer, Japan, pp 1203–1240
10. Challis GL (2008) Mining microbial genomes for new natural products and biosynthetic pathways. Microbiology 154:1555–1569
11. Challis GL, Hopwood DA (2003) Synergy and contingency as driving forces for the evolution of multiple secondary metabolite production by Streptomyces species. Proc Natl Acad Sci U S A 100(Suppl 2):14555–14561
12. Charlop-Powers Z, Owen JG, Reddy BVB, Ternei MA, Guimaraes DO, de Frias UA, Pupo MT, Seepe P, Feng Z, Brady SF (2015) Global biogeographic sampling of bacterial secondary metabolism. eLife 4:e05048. doi:10.7554/eLife.05048
13. de la Cruz F, Davies J (2000) Horizontal gene transfer and the origin of species: lessons from bacteria. Trends Microbiol 8:128–133
14. Donadio S, Monciardina P, Sosio M (2007) Polyketide synthases and nonribosomal peptide synthetases: the emerging view from bacterial genomics. Nat Prod Rep 24:1073–1109
15. Doroghazi JR, Metcalf WW (2013) Comparative genomics of actinomycetes with a focus on natural product biosynthetic genes. BMC Genomics 14:611. doi:10.1186/1471-2164-14-611
16. Duan YY, Ming H, Dong L, Yin YR, Zhang Y, Zhou EM, Liu L, Nie GX, Li WJ (2014) Streptomyces calidiresistens sp. nov., isolated from a hot spring sediment. Antonie Van Leeuwenhoek 106:189–196
17. Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–79
18. Gottardi EM, Krawczyk JM, von Suchodoletz H, Schadt S, Muhlenweg A, Uguru GC, Plezer S, Fiedler HP, Bibb MJ, Stach JEM, Suusmuth RD (2011) Abyssomicin biosynthesis: formation of an unusual polyketide, antibiotic feeding studies and genetic analysis. ChemBioChem 12:1401–1410
19. Hanshew AS, McDonald BR, Diaz CD, Dijeto-Lordon C, Blatrix R, Currie CR (2015) Characterization of actinobacteria associated with three ant-plant mutualisms. Microb Ecol 69:192–203
20. Hedlund BP, Cole JK, Williams AJ, Hou W, Zhou E, Li W, Dong H (2012) A review of the microbiology of the Rehai geothermal field in Tengchong, Yunnan Province, China. Geosci Front 3:273–288
21. Hedlund BP, Reysenbach AL, Huang L, Ong JC, Liu Z, Dodsworth JA, Ahmed R, Williams AJ, Briggs BR, Liu Y, Hou W, Dong H (2015) Isolation of diverse members of the Aquificales from geothermal springs in Tengchong, China. Front Microbiol 6:157. doi:10.3389/fmicb.2015.00157
22. Holmes AJ, Bowyer J, Holley MP, O’Donoghue M, Montgomery M, Gilings MR (2000) Diverse, yet-to-be-cultured members of the Rubrobacter subdivision of the Actinobacteria are widespread in Australian arid soils. FEMS Microbiol Ecol 33:111–120
23. Hotopp JCD (2011) Horizontal gene transfer between bacteria and animals. Trends Genet 27:157–163
24. Hugo WB, Russell AD (1983) Pharmaceutical microbiology, 3rd edn. Blackwell, Oxford
25. Ikeda H, Ishikawa J, Hanamoto A, Shinose M, Kikuchi H, Shiba T, Sakaki Y, Hattori M, Omura S (2003) Complete genome sequence and comparative analysis of the industrial microorganism Streptomyces avermitilis. Nat Biotechnol 21:526–531
26. Jami M, Ghanbari M, Kneifel W, Domig KJ (2015) Phylogenetic diversity and biological activity of culturable actinobacteria isolated form freshwater fish gut microbiota. Microbiol Res 175:6–15
27. Jiao JY, Liu L, Zhou EM, Wei DQ, Ming H, Xian WD, Yuan CG, Zhong JM, Li WJ (2015) Actinomadura amylolytica sp. nov. and Actinomadura cellulosilytica sp. nov., isolated from geothermally heated soil. Antonie Van Leeuwenhoek 108:75–83
28. Kim JH, Feng Z, Bauer JD, Kallifidas D, Calle PY, Brady SF (2010) Cloning large natural product gene clusters from the environment: piecing environmental DNA gene clusters back together with TAR. Biopolymers 93:833–844
29. Kim OS, Cho YJ, Lee K, Yoon SH, Kim M, Na H, Park SC, Jeon YS, Lee JH, Yi H, Won S, Chun J (2012) Introducing EzTaxon-e: a prokaryotic 16S rRNA gene sequence database with phylotypes that represent uncultured species. Int J Syst Evol Microbiol 62:716–721
30. Kimura M (1980) A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–130
31. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23:2947–2948
32. Li J, Zhao GZ, Huang HY, Qin S, Zhu WY, Zhao LX, Xu LH, Zhang S, Li WJ, Strobel G (2012) Isolation and characterization of culturable endophytic actinobacteria associated with Artemisia annua L. Antonie Van Leeuwenhoek 101:515–527
33. Li WJ, Xu P, Schumann P, Zhang YQ, Pukall R, Xu LH, Stackebrandt E, Jiang CL (2007) Georgenia ruanii sp. nov., a novel actinobacterium isolated from forest soil in Yunnan (China) and emended description of the genus Georgenia. Int J Syst Evol Microbiol 57:1424–1428
34. Li Y, Li Z, Yamanaka K, Xu Y, Zhang W, Vlamakis H, Kolter R, Moore BS, Qian PY (2015) Directed natural product biosynthesis gene cluster capture and expression in the model bacterium Bacillus subtilis. Sci Rep 5:9383. doi:10.1038/srep09383
35. Luo K (2010) Screening of PKS gene from soil metagenomics library and identification of the active substance against nematode. Plant Protection (in chinese) 36:5. doi:10.3969/j.issn.0529-1542.2010.05.008
36. Manivasagan P, Venkatesan J, Kim SK (2013) Introduction to marine actinobacteria. In: Kim SK (ed.). Marine Microbiology: Bioactive Compounds and Biotechnological Applications, 1st edn. Wiley-VCH Verlag GmbH & Co, KGaA, pp 1–19
37. Metsä-Ketelä M, Salo V, Halo L, Hautala A, Hakala J, Mäntsälä P, Ylihonko K (1999) An efficient approach for screening minimal PKS genes from Streptomyces. FEMS Microbiol Lett 180:1–6
38. Moffitt MC, Neilan BA (2001) On the presence of peptide synthetase and polyketide synthase genes in the cyanobacterial genus Nodularia. FEMS Microbiol Lett 196:207–214
39. Moffitt MC, Neilan BA (2003) Evolutionary affiliations within the superfamily of ketosynthases reflect complex pathway associations. J Mol Evol 56:446–457
40. Neilan BA, Dittmann E, Rouhiainen L, Bass RA, Schaub V, Sivonen K, Borner T (1999) Nonribosomal peptide synthesis and toxigenicity of cyanobacteria. J Bacteriol 181:4089–4097
41. Nimaichand S, Devi AM, Tamreihao K, Ningthoujam DS, Li WJ (2015) Actinobacterial diversity in limestone deposit sites in Hundung, Manipur (India) and their antimicrobial activities. Front Microbiol 6:413. doi:10.3389/fmicb.2015.00413
42. Omura S, Ikeda H, Ishikawa J, Hanamoto A, Takahashi C, Shinose M, Takahashi Y, Horikawa H, Nakazawa H, Osonoe T, Kikuchi H, Shiba T, Sakaki Y, Hattori M (2001) Genome sequence of an industrial microorganism Streptomyces avermitilis: deducing the ability of producing secondary metabolites. Proc Natl Acad Sci U S A 98:12215–12220
43. Parveen B, Reveilliez JP, Mary I, Ravet V, Bronner G, Mangot JF, Domaizon I, Debroas D (2011) Diversity and dynamics of free-living and particle-associated betaproteobacteria and Actinobacteria in relation to phytoplankton and zooplankton communities. FEMS Microbiol Ecol 77:461–476
44. Qin S, Li J, Chen HH, Zhao GZ, Zhu WY, Jiang CL, Xu LH, Li WJ (2009) Isolation, diversity, and antimicrobial activity of rare actinobacteria from medicinal plants of tropical rain forests in Xishuangbanna, China. Appl Environ Microbiol 75:6176–6186
45. Riedlinger J, Reicke A, Zahner H, Krismer B, Bull AT, Maldonado LA, Ward AC, Goodfellow M, Bister B, Bischoff D, Sussmuth RD, Fiedler HP (2004) Abyssomicins, inhibitors of the para-aminobenzoic acid pathway produced by the marine Verrucosispora strain AB-18-032. J Antibiot 57:271–279
46. Rutledge PJ, Challis GL (2015) Discovery of microbial natural products by activation of silent biosynthetic gene clusters. Nat Rev Microbiol 13:509–523
47. Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425
48. Schneemann I, Nagel K, Kajahn I, Labes A, Wiese J, Imhoff JF (2010) Comprehensive investigation of marine actinobacteria associated with the sponge Halichondria panicea. Appl Environ Microbiol 76:3702–3714
49. Song ZQ, Chen JQ, Jiang HC, Zhou EM, Tang SK, Zhi XY, Zhang LX, Zhang CL, Li WJ (2010) Diversity of Crenarchaeoto in terrestrial hot springs in Tengchong, China. Extremophiles 14:287–296
50. Song ZQ, Zhi XY, Li WJ, Jiang HC, Zhang CL, Dong HL (2009) Actinobacterial diversity in hot springs in Tengchong (China), Kamchatka (Russia), and Nevada (USA). Geomicrobiol J 26:256–263
51. Sun W, Zhang F, He L, Karthik L, Li Z (2015) Actinomycetes from the South China Sea sponges: isolation, diversity, and potential for aromatic polyketides discovery. Front Microbiol 6:1048. doi:10.3389/fmicb.2015.01048
52. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2011) MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Mol Biol Evol 30:2725–2729
53. Udikovic-Kolic N, Wichmann F, Broderick NA, Handelsman J (2014) Bloom of resident antibiotic-resistant bacteria in soil following manure fertilization. Proc Natl Acad Sci U S A 111:15202–15207
54. Vernon TR (1955) Spore formation in the genus Streptomyces. Nature 176:935–936
55. Zerikly M, Challis GL (2009) Strategies for the discovery of new natural products by genome mining. Chembiochem 10:625–633
56. Zhou EM, Tang SK, Sjoholm C, Song ZQ, Yu TT, Yang LL, Ming H, Nie GX, Li WJ (2012) Thermoactinospora rubra gen. nov., sp., nov., a thermophilic actinomycete isolated from Tengchong, Yunnan province, south-west China. Antonie Van Leeuwenhoek 102:177–185
57. Zhou EM, Yang LL, Song ZQ, Yu TT, Nie GX, Ming H, Zhou Y, Tang SK, Li WJ (2012) Thermocatellispora tengchongensis gen. nov., sp. nov., a new member of the family Streptosporangiaceae. Int J Syst Evol Microbiol 62:2417–2423