Abstract
A Streptomyces strain isolated from a mangrove sediment was classified using a polyphasic approach. The organism, isolate GY1T, was found to have chemical and morphological properties typical of members of the genus Streptomyces. The isolate was shown to form a distinct phyletic line within the Streptomyces radiopugnans 16S rRNA gene subclade and to be closely related to the type strain of Streptomyces fenhuangensis (98.7 % similarity). It is also closely related to the type strain of Streptomyces bakulensis which was also closely related to members of the Streptomyces glaucosporus 16S rRNA gene subclade. Isolate GY1T was distinguished readily from the S. barkulensis type strain and from species classified in the S. radiopugnans clade using a combination of morphological and physiological properties, including a requirement for seawater for growth. Based on the genotypic and phenotypic data, it is proposed that isolate GY1T (=NCIMB 14980T, NRRL B-69296T) be classified in the genus Streptomyces as Streptomyces mangrovi sp. nov.
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Ahmed L, Jensen PR, Freel KC, Brown R, Al Jones, Kim B-Y, Goodfellow M (2013) Salinispora pacifica sp. nov., an actinomycete from marine sediments. Antonie Van Leeuwenhoek 103:1069–1078
Antony-Babu S, Goodfellow M (2008) Biosystematics of alkaliphilic streptomycetes isolated from seven locations across a beach and dune system. Antonie Van Leeuwenhoek 94:581–591
Bérdy J (2012) Thoughts and facts about antibiotics; where we are now and where are we heading. J Antibiot (Tokyo) 51:1–26
Busti E, Monciardini P, Cavaletti L, Bamonte R, Lazzarini A, Sosio M, Donadio S (2006) Antibiotic-producing ability by representatives of newly discovered lineages of actinomycetes. Microbiology 152:675–683
Carro L, Zūníga P, de la Calle F, Trujillo ME (2012) Streptomyces pharmamarensis sp. nov. isolated from a marine sediment. Int J Syst Evol Microbiol 62:1165–1170
Collins MD (1994) Isoprenoid quinones. In: Goodfellow M, O’Donnell AG (eds) Chemical methods in prokaryotic systematics. Wiley Colchester, Chichester, pp 265–309
Felsenstein J (1981) Evolutionary trees from DNA sequences: a maximum-likelihood approach. J Mol Evol 17:368–376
Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791
Fiedler H-P, Bruntner C, Bull AT, Ward AC, Goodfellow M, Potterat O, Puder C, Mihm M (2005) Marine actinomycetes as a source of novel secondary metabolites. Antonie Van Leeuwenhoek 87:37–42
Fitch WM (1971) Towards designing a course of evolution: minimum change for a specific tree topology. Syst Zool 20:406–416
Goodfellow M (2012) Phylum XXVI. Actinobacteria phyl. nov. In: Goodfellow M, Kämpfer P, Busse H-J, Trujillo ME, Suzuki K-I, Ludwig W, Whitman WB (eds) Bergey’s manual of systematic bacteriology, Part A. Springer, New York, pp 33–34
Goodfellow M, Fiedler H-P (2010) A guide to successful bioprospecting: informed by actinobacterial systematics. Antonie Van Leeuwenhoek 98:119–142
Goodfellow M, Haynes JA (1984) Actinomycetes in marine sediments. In: Ortiz-Ortiz L, Bojalil L, Yakoleff V (eds) Biological, biochemical and biomedical aspects of actinomycetes. Academic Press, Inc., Orlando, pp 453–472
Guidon S, Gascuel O (2003) A simple, fast and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704
Han KH, Nedashkovskaya OI, Milhailov VV, Kim SB, Bae KS (2003) Salinibacterium amurskiense gen. nov., a novel genus of the family Microbacteriaceae from the marine environment. Int J Syst Evol Microbiol 53:2061–2066
Hasegawa T, Takizawa M, Tanida S (1983) A rapid analysis for chemical grouping of aerobic actinomycetes. J Gen Appl Microbiol 29:319–322
Hong K, Gao A-H, Xie Q-Y, Gao H, Zhuang L, Lin H-P, Yu H-P, Li J, Yao X-S, Goodfellow M, Ruan J-S (2009) Actinomycetes for marine drug discovery isolated from mangrove soils and plants in China. Mar Drugs 7:24–44
Hu H, Lin H-P, Xie Q, Li L, Xie S-Q, Sun M, Hong K (2011) Streptomyces shenzhenensis sp. nov., a novel actinomycete isolated from mangrove sediment. Antonie Van Leeuwenhoek 100:631–637
Hughes CC, Fenical W (2010) Actinobacteria from the sea. Chemistry 16:12512–12525
Jensen PR, Dwight R, Fenical W (1991) Distribution of actinomycetes in near-shore tropical marine sediments. Appl Environ Microbiol 57:1102–1108
Jukes TH, Cantor CR (1969) Evolution of protein molecules. In: Munro HN (ed) Mammalian protein metabolism. Academic Press, London, pp 21–132
Kämpfer P (2012) Genus Streptomyces Waksman and Henrici 1943, 339AL, emend Witt and Stackebrandt 1990, 370, emend Wellington, Stackebrandt, Sanders, Wolstrup and Jorgensen 1992, 159. In: Goodfellow M, Kämpfer P, Busse H-J, Trujillo ME, Suzuki K-I, Ludwig W, Whitman WB (eds) Bergey’s manual of systematic bacteriology, Part B. Springer, New York, pp 1455–1767
Kawato M, Shinobu R (1959) On Streptomyces herbaricolor sp. Mem Osaka Univ Lib Arts Educ B 8:114
Kelly KL (1964) Inter-society color council-national bureau of standards color-charts illustrated with centroid colours. US Government Printing Office, Washington
Khan ST, Tamura T, Takagi M, Shin-ya K (2010) Streptomyces tateyamensis sp. nov., Streptomyces marinus sp. nov. and Streptomyces haliclonae sp. nov. isolated from the marine sponge Haliclona sp. Int J Syst Evol Microbiol 60:2775–2779
Kim S-B, Goodfellow M (2002) Streptomyces thermospinisporus sp. nov. a moderately thermophilic carboxydotrophic streptomycete isolated from soil. Int J Syst Microbiol 52:1125–1128
Kim O-S, Cho YJ, Lee K, Yoon S-H, Kim M, Na H, Park SC, Yeon 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
Kroppenstedt RM (1995) Fatty acid and menaquinone analysis of actinomycetes and related organisms. In: Goodfellow M, Minnikin DE (eds) Chemical methods in bacterial systematics. Academic Press, London, pp 179–199
Labeda DP, Goodfellow M, Brown R, Ward AC, Lanoot C, Vancanneyt M, Swings J, Kim S-B, Liu Z, Chun J, Tamura T, Oguchi A, Kikuchi T, Kikuchi H, Nishii T, Tsuji K, Yamaguichi Y, Tase A, Takahashi M, Sakane T, Suzuki KI, Hatano K (2012) Phylogenetic study of the species within the family Streptomycetaceae. Antonie Van Leeuwenhoek 101:73–104
Lechevalier MP, Lechevalier H (1970) Chemical composition as a criterion in the classification of aerobic actinomycetes. Int J Syst Evol Microbiol 20:435–443
Lechevalier MP, De Biévre C, Lechevalier HA (1977) Chemotaxonomy of aerobic actinomycetes, phospholipid composition. Biochem Syst Evol 5:248–260
Maldonado L, Fenical W, Goodfellow M, Jensen PR, Kauffman CK, Ward AC (2005) Salinispora gen. nov., Salinispora arenicola sp. nov., Salinispora tropica asp. nov., obligate marine actinomycetes belonging to the family Micromonosporaceae. Int J Syst Evol Microbiol 55:1759–1766
Mao J, Tang Q, Zhang Z, Wang W, Wei D, Huang Y, Liu Z, Shi Y, Goodfellow M (2007) Streptomyces radiopugnans sp. nov., a radiation-resistant actinomycete isolated from radiation polluted soil in China. Int J Syst Evol Microbiol 57:2578–2582
Meier-Kolthoff JP, Göker M, Spöer C, Klenk H-P (2013) When should a DDH experiment be mandatory in microbial taxonomy? Arch Microbiol 95:413–418
Minnikin DE, O’Donnell AG, Goodfellow M, Alderson G, Athalye M, Schaal A, Parlett JH (1984) An integrated procedure for the extraction of bacterial isoprenoid quinones and polar lipids. J Microbiol Methods 2:233–241
O’Donnell AG, Falconer C, Goodfellow M, Ward AC, Williams E (1993) Biosystematics and diversity amongst novel carboxydotrophic actinomycetes. Antonie Van Leeuwenhoek 64:325–340
Okami Y, Okazaki T (1972) Studies on marine microorganisms 1. Actinomycetes in Sagami Bay and their antibiotic substances. J Antibiot (Tokyo) 25:456–460
Okoro CK, Brown R, Jones AL, Andrews BA, Asenjo JA, Goodfellow M, Bull AT (2009) Diversity of culturable actinomycetes in hyper-arid soils of the Atacama Desert, Chile. Antonie Van Leeuwenhoek 95:121–133
Parte AC (2013) LPSN-list of prokaryotic names with standing in nomenclature. Nucleic Acids Res 42:D613–D616
Phongsopitanun W, Thawai C, Suwanborirux K, Kudo T, Ohkuma M, Tanasupawat S (2014) Streptomyces chumphonensis sp. nov., isolated from marine sediements. Int J Syst Evol Microbiol 64:2605–2610
Pimentel-Elardo SM, Scheuemayer M, Kozytska S, Hentschel U (2009) Streptomyces axinellae sp. nov. isolated from the Mediterranean sponge Axinella polypoides (Porifera). Int J Syst Evol Microbiol 59:1433–1437
Ray L, Mishra SR, Panda AN, Rastogi G, Pattanaik AK, Adhya TK, Suar M, Raina V (2014) Streptomyces barkulensis sp. nov., isolated from an estuarine lake. Int J Syst Evol Microbiol 64:1365–1372
Saitou N, Nei M (1987) The neighbor-joining method: a new method for constructing phylogenetic trees. Mol Biol Evol 4:406–425
Santhanam R, Okoro CK, Rong X, Huang Y, Bull AT, Weon H-Y, Andrews BA, Asenjo JA, Goodfellow M (2012) Streptomyces atacamensis sp. nov., isolated from an extreme hyper-arid soil of the Atacama Desert. Chile. Int J Syst Evol Microbiol 62:2680–2684
Sasser M (1990) Identification of bacteria by gas chromatography of cellular fatty acids. MIDI Technical Note 101 MIDI Inc
Shirling EB, Gottlieb D (1966) Methods for characterization of Streptomyces species. Int J Syst Bacteriol 16:313–340
Songsumanus A, Tanasupawat S, Igarashi Y, Kudo T (2013) Micromonospora maritima sp. nov., isolated from mangrove soil. Int J Syst Evol Microbiol 63:554–559
Sui J-L, Xu X-X, Qu Z, Wang H-L, Lin H-P, Xie Q-Y, Ruan J-S, Ruan J-S, Hong K (2011) Streptomyces sanyensis sp. nov., isolated from mangrove sediment. Int J Syst Evol Microbiol 61:1632–1637
Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) Mega 6: molecular evolutionary genetics analysis version 6. Mol Biol Evol 30:2725–2729
Tan GYA, Robinson S, Lacey E, Goodfellow M (2006) Exploration of Amycolatopsis diversity in soil using genus specific primers and novel selective media. Syst Appl Microbiol 29:557–569
Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680
Tian X-P, Long L-J, Wang F-Z, Xu Y, Li J, Zhang J, Zhang C-S, Zhang S, Li W-J (2012a) Streptomyces nanhaiensis sp. nov., a marine streptomycete isolated from a deep-sea sediment. Int J Syst Evol Microbiol 62:864–868
Tian X-P, Xu Y, Zhang J, Li J, Chen Z, Kim C-J, Li W-J, Zhang C-S, Zhang S (2012b) Streptomyces oceani sp. nov., a new obligate marine actinomycete isolated from a deep-sea sample of seep authigenic carbonate nodule in South China Sea. Antonie van Leuewenhoek 102:335–343
Veyisoglu A, Sahin N (2014) Streptomyces hoynatensis sp. nov., isolated from deep marine sediment. Int J Syst Evol Microbiol 64:819–826
Wayne LG, Brenner DJ, Colwell RR, Grimont PAD, Kandler O, Krichevsky MI, Moore LH, Moore WEC, Murray RGE et al (1987) International Committee on Systematic Bacteriology. Report of the ad hoc committee on reconciliation of approaches to bacterial systematics. Int J Syst Bacteriol 37:463–464
Weyland H (1981) Distribution of actinomycetes on the sea-floor. Zbl Bakt Suppl 11:185–193
Williams ST, Goodfellow M, Alderson G, Wellington EMH, Sneath PHA, Sackin MJ (1983) Numerical classification of Streptomyces and related genera. J Gen Microbiol 129:1743–1813
Xiao J, Wang Y, Luo Y, Xie S-J, Ruan J-S, Xu J (2009) Streptomyces avicenniae sp. nov., a novel actinomycete isolated from the rhizosphere of the mangrove plant Avicenna mariana. Int J Syst Evol Microbiol 59:2624–2628
Zhu H, Jiang S, Yao O, Wang Y, Chen M, Chen Y, Guo J (2011) Streptomyces fenghuangensis sp. nov., isolated from seawater. Int J Syst Evol Microbiol 61:2811–2815
Zotchev SB (2012) Marine actinomycetes as an emerging resource for the drug development pipelines. J Biotechnol 158:168–175
Acknowledgments
Ghada Yousif is grateful for support from the Egyptian Government to allow her to study in the UK on a ParOwn scholarship and for advice from Wael Hozzein and from her master supervisors Medhat abdel Fattah, Sherif Hassan and Ahmed Reyad. Kanungnid Busarakam gratefully thanks the Thai Royal Government for a scholarship.
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Yousif, G., Busarakam, K., Kim, BY. et al. Streptomyces mangrovi sp. nov., isolated from mangrove forest sediment. Antonie van Leeuwenhoek 108, 783–791 (2015). https://doi.org/10.1007/s10482-015-0533-0
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DOI: https://doi.org/10.1007/s10482-015-0533-0