Ecological Strategies Behind the Selection of Cultivable Actinomycete Strains from the Yucatan Peninsula for the Discovery of Secondary Metabolites with Antibiotic Activity

Microbial Ecology - Tập 77 - Trang 839-851 - 2019
Yessica Parera-Valadez1, Alejandro Yam-Puc1, Lluvia Korynthia López-Aguiar1, Rocío Borges-Argáez2, Mario Alberto Figueroa-Saldivar3, Mirbella Cáceres-Farfán2, Norma Angélica Márquez-Velázquez1, Alejandra Prieto-Davó1
1Laboratorio de Ecología Microbiana y Productos Naturales Marinos, Unidad de Química en Sisal, Facultad de Química, Universidad Nacional Autónoma de México, Sisal, Mexico
2CICY - Centro de Investigación Científica de Yucatán, Mérida, Mexico
3Departamento de Farmacia, Facultad de Química, Universidad Nacional Autónoma de México, Mexico City, Mexico

Tóm tắt

The quest for novel natural products has recently focused on the marine environment as a source for novel microorganisms. Although isolation of marine-derived actinomycete strains is now common, understanding their distribution in the oceans and their adaptation to this environment can be helpful in the selection of isolates for further novel secondary metabolite discovery. This study explores the taxonomic diversity of marine-derived actinomycetes from distinct environments in the coastal areas of the Yucatan Peninsula and their adaptation to the marine environment as a first step towards novel natural product discovery. The use of simple ecological principles, for example, phylogenetic relatedness to previously characterized actinomycetes or seawater requirements for growth, to recognize isolates with adaptations to the ocean in an effort to select for marine-derived actinomycete to be used for further chemical studies. Marine microbial environments are an important source of novel bioactive natural products and, together with methods such as genome mining for detection of strains with biotechnological potential, ecological strategies can bring useful insights in the selection and identification of marine-derived actinomycetes for novel natural product discovery.

Tài liệu tham khảo

Kong DX, Jiang YY, Zhang HY (2010) Marine natural products as sources of novel scaffolds: achievement and concern. Drug Discov Today 15(21–22):884–886. https://doi.org/10.1016/j.drudis.2010.09.002.

Mayer AM, Glaser KB, Cuevas C, Jacobs RS, Kem W, Little RD, McIntosh JM, Newman DJ, Potts BC, D S (2010) The odyssey of marine pharmaceuticals: a current pipeline perspective. - PubMed - NCBI. Trends Pharmacol Sci 31(6):255–265. https://doi.org/10.1016/j.tips.2010.02.005

Martins A, Vieira H, Gaspar H, Santos S (2014) Marketed marine natural products in the pharmaceutical and cosmeceutical industries: tips for success. Mar Drugs 12(2):1066–1101. https://doi.org/10.3390/md12021066

Subramani R, Aalbersberg W (2012) Marine Actinomycetes: an ongoing source of novel bioactive metabolites. Microbiol Res 167(10):571–580. https://doi.org/10.1016/j.micres.2012.06.005

Manivasagan P, Venkatesa J, Kim S.-K. Marine microbiology: bioactive compounds and biotechnological applications. Wiley-VCH Verlag GmbH & Co. KGaA . 2013. pp. 1–19.

Manivasagan P, Venkatesan J, Sivakumar K, Kim S-K (2014) Pharmaceutically active secondary metabolites of marine Actinobacteria. Microbiol Res 169(4):262–278. https://doi.org/10.1016/j.micres.2013.07.014

Sharma R, Ranjan R, Kapardar RK, Grover A (2005) Special section: microbial diversity “unculturable” bacterial diversity: an untapped resource. Curr Sci 89(1)

Kyrpides NC, Hugenholtz P, Eisen JA, Woyke T, Göker M, Parker CT, Amann R, Beck BJ, Chain PSG, Chun J, Colwell RR, Danchin A, Dawyndt P, Dedeurwaerdere T, DeLong EF, Detter JC, De Vos P, Donohue TJ, Dong X-Z, Ehrlich DS, Fraser C, Gibbs R, Gilbert J, Gilna P, Glöckner FO, Jansson JK, Keasling JD, Knight R, Labeda D, Lapidus A, Lee J-S, Li W-J, MA J, Markowitz V, Moore ERB, Morrison M, Meyer F, Nelson KE, Ohkuma M, Ouzounis CA, Pace N, Parkhill J, Qin N, Rossello-Mora R, Sikorski J, Smith D, Sogin M, Stevens R, Stingl U, Suzuki K, Taylor D, Tiedje JM, Tindall B, Wagner M, Weinstock G, Weissenbach J, White O, Wang J, Zhang L, Zhou Y-G, Field D, Whitman WB, Garrity GM, Klenk H-P, Pace N, Achtman M, Wagner M, Pace N, Whitman W, Coleman D, Wiebe W, López-García P, Rodríguez-Valera F, Pedrós-Alió C, Moreira D, Amann R, Ludwig W, Schleifer K, Hugenholtz P, Rappé M, Giovannoni S, Kyrpides N, Hugenholtz P, Kyrpides N, Woese C, Pagani I, Liolios K, Jansson J, Chen I, Smirnova T, Tindall B, Rosselló-Móra R, Busse H, Ludwig W, Kämpfer P, Trüper H, Euzéby J, Tindall B, Kämpfer P, Euzéby J, Oren A, Tindall B, Garrity G, Chain P, Grafham D, Fulton R, Fitzgerald M, Hostetler J, Göker M, Klenk H, Wu D, Hugenholtz P, Mavromatis K, Pukall R, Dalin E, Shih P, Wu D, Latifi A, Axen S, Fewer D, Rinke C, Schwientek P, Sczyrba A, Ivanova N, Anderson I, Nelson K, Weinstock G, Highlander S, Worley K, Creasy H, Field D, Amaral-Zettler L, Cochrane G, Cole J, Dawyndt P, Field D, Garrity G, Gray T, Morrison N, Selengut J, Field D, Sansone S, Collis A, Booth T, Dukes P, Yilmaz P, Kottmann R, Field D, Knight R, Cole J, Walker A, Göker M, Klenk H, Buckley M, Roberts R, Garrity G, Field D, Kyrpides N, Hirschman L, Sansone S, Garrity G, Wilke A, Harrison T, Wilkening J, Field D, Glass E, Yarza P, Richter M, Peplies J, Euzeby J, Amann R, Dedeurwaerdere T, DeVos P, Dijkshoorn L, Connon S, Giovannoni S, Staley J, Konopka A, Faith D, Qin J, Li R, Raes J, Arumugam M, Burgdorf K, Gilbert J, Meyer F, Jansson J, Gordon J, Pace N (2014) Genomic encyclopedia of bacteria and archaea: sequencing a myriad of type strains. PLoS Biol 12(8):e1001920. https://doi.org/10.1371/journal.pbio.1001920

Pye CR, Bertin MJ, Lokey RS, Gerwick WH, Linington RG (2017) Retrospective analysis of natural products provides insights for future discovery trends. Proc Natl Acad Sci U S A 114(22):5601–5606. https://doi.org/10.1073/pnas.1614680114

Gomez-Escribano JP, Alt S, Bibb MJ (2016) Next generation sequencing of Actinobacteria for the discovery of novel natural products. Mar Drugs 14(4):6–8. https://doi.org/10.3390/md14040078.

Jensen PR, Dwight R, Fenical W (1991) Distribution of actinomycetes in near-shore tropical marine sediments, 57 (4).

Mincer TJ, Jensen PR, Kauffman CA, Fenical W (2002) Widespread and persistent populations of a major new marine actinomycete taxon in ocean sediments widespread and persistent populations of a major new marine actinomycete taxon in ocean sediments. Appl Environ Microbiol 68(10):5005–5011. https://doi.org/10.1128/AEM.68.10.5005.

Prieto-Davo A (2013) Phylogenetic and chemical diversity of marine-derived actinomycetes from Southern California sediments. University of California

Prieto-Davo A, Dias T, Gomes SE, Rodrigues S, Parera-Valadez Y, Borralho PM, Pereira F, Rodrigues CMP, Santos-Sanches I, Gaudencio SP (2016) The Madeira Archipelago as a significant source of marine-derived actinomycete diversity with anticancer and antimicrobial potential. Front Microbiol 7(OCT):1–12. https://doi.org/10.3389/fmicb.2016.01594.

Fenical W (1994) Strategies for the discovery of secondary metabolites from marine bacteria: ecological perspectives. Annu Rev Microbiol 48:559–584. https://doi.org/10.1146/annurev.micro.48.1.559

Netzker T, Fischer J, Weber J, Mattern DJ, König CC, Valiante V, Schroeckh V, Brakhage AA (2015) Microbial communication leading to the activation of silent fungal secondary metabolite gene clusters. Front Microbiol 6:299. https://doi.org/10.3389/fmicb.2015.00299

Lam KS (2006) Discovery of novel metabolites from marine actinomycetes. Curr Opin Microbiol 9(3):245–251. https://doi.org/10.1016/j.mib.2006.03.004

Ragini K, Aalbersberg W (2014) Isolation and characterisation of rifamycin W and phenylethylamides from a Fijian marine actinomycete Salinispora arenicola. South Pacific J Nat Appl Sci 32(2):43. https://doi.org/10.1071/SP14007

El Naggar MM, El-Assar SA, Shata AMA (2015) Production of antitumor agents from novel marine actinomycetes isolated from Alexandria, Egypt. Single Cell Biol 4(1). https://doi.org/10.4172/2168-9431.1000e122.

Sanjivkumar M, Ramesh Babu D, Sunganya AM, Silambarasan AM, Balagurunathan R, Immanuel G (2016) Investigation on pharmacological activities of secondary metabolite extracted from a mangrove associated actinobacterium Streptomyces olivaceus (MSU3). Biocatal Agric Biotechnol 6:82–90. https://doi.org/10.1016/J.BCAB.2016.03.001.

Kumar KN, Elavarasi TGA (2013) Studies on antimicrobial activity of marine actinomycetes isolated from Rameswaram , 4 (4), 706–710.

Messaoudi O, Bendahou M, Benamar I, Abdelwouhud D (2015) Identification and preliminary characterization of non-polyene antibiotics secreted by new strain of actinomycete isolated from Sebkha of Kenadsa, Algeria. Asian Pac J Trop Biomed 5(6):438–445. https://doi.org/10.1016/J.APJTB.2015.04.002

Bauer-Gottwein P, Gondwe BRN, Charvet G, Marín LE, Rebolledo-Vieyra M, Merediz-Alonso G (2011) Review: the Yucatán Peninsula karst aquifer, Mexico. Hydrogeol J 19(3):507–524. https://doi.org/10.1007/s10040-010-0699-5

Pérez L, Bugja R, Lorenschat J, Brenner M, Curtis J, Hoelzmann P, Islebe G, Scharf B, Schwalb A (2011) Aquatic ecosystems of the Yucatán Peninsula (Mexico), Belize, and Guatemala. Hydrobiologia 661(1):407–433. https://doi.org/10.1007/s10750-010-0552-9

Lozupone C, Knight R (2005) UniFrac: a new phylogenetic method for comparing microbial communities. Appl Environ Microbiol 71(12):8228–8235. https://doi.org/10.1128/AEM.71.12.8228-8235.2005

Kock I, Maskey RP, Biabani MAF, Helmke E, Laatsch H (2005) 1-Hydroxy-1-norresistomycin and resistoflavin methyl ether: new antibiotics from marine-derived streptomycetes. J Antibiot (Tokyo) 58(8):530–534. https://doi.org/10.1038/ja.2005.73

Mohanraj G, Sekar T (2013) Isolation and screening of actinomycetes from marine sediments for their potential to produce antimicrobials. Int J life Sci Biotechnol pharma Res 2(3):115–126

Fenical W, Jensen PR (2006) Developing a new resource for drug discovery: marine actinomycete bacteria. Nat Chem Biol 2(12):666–673. https://doi.org/10.1038/nchembio841

Tiwari K, Gupta RK (2012) Rare actinomycetes: a potential storehouse for novel antibiotics. Crit Rev Biotechnol 32(2):108–132. https://doi.org/10.3109/07388551.2011.562482

Liu X, Ashforth E, Ren B, Song F, Dai H, Liu M, Wang J, Xie Q, Zhang L (2010) Bioprospecting microbial natural product libraries from the marine environment for drug discovery. J Antibiot (Tokyo) 63(8):415–422. https://doi.org/10.1038/ja.2010.56

Hugenholtz P, Hooper SD, Kyrpides NC (2009) Focus: synergistetes: genomics update. Environ Microbiol 11(6):1327–1329. https://doi.org/10.1111/j.1462-2920.2009.01949.x

Milshteyn A, Schneider JS, Brady SF (2014) Mining the metabiome: identifying novel natural products from microbial communities. Chem Biol 21(9):1211–1223. https://doi.org/10.1016/j.chembiol.2014.08.006

Crüsemann M, O’Neill EC, Larson CB, Melnik AV, Floros DJ, Da Silva RR, Jensen PR, Dorrestein PC, Moore BS (2017) Prioritizing natural product diversity in a collection of 146 bacterial strains based on growth and extraction protocols. J Nat Prod 80(3):588–597. https://doi.org/10.1021/acs.jnatprod.6b00722

Rojas-Herrera R, Zamudio-Maya M, Arena-Ortiz L, Pless R, O’Connor-Sánchez A (2011) Microbial diversity, metagenomics and the Yucatán aquifer. Divers. microbiana, metagenómica y el acuífero Yucatán, 80 (130), 231–240.

Maldonado L, Fragoso-Yáñez D, Pérez-García A, Rosellón-Druker J, Quintana ET (2009) Actinobacterial diversity from marine sediments collected in Mexico. Antonie Van Leeuwenhoek 95(2):111–120. https://doi.org/10.1007/s10482-008-9294-3

Martin GD a, Tan LT, Jensen PR, Dimayuga RE, Fairchild CR, Raventos-Suarez C, Fenical W (2007) Marmycins A and B, cytotoxic pentacyclic C-glycosides from a marine sediment-derived actinomycete related to the genus Streptomyces. J Nat Prod 70(9):1406–1409. https://doi.org/10.1021/np060621r

Maldonado L a, Fenical W, Jensen PR, Kauffman C a, Mincer TJ, Ward AC, Bull AT, Goodfellow M (2005) Salinispora arenicola gen. nov., sp. nov. and Salinispora tropica sp. nov., obligate marine actinomycetes belonging to the family Micromonosporaceae. Int J Syst Evol Microbiol 55:1759–1766. https://doi.org/10.1099/ijs.0.63625-0

Torres-Beltrán M (2012) Evaluation of the Gulf of California as a potential source of bioactive marine Actinobacteria. Ciencias Mar 38(4):609–624. https://doi.org/10.7773/cm.v38i4.2131

Goodfellow M, Kämpfer P, Hans-Jürgen B, Trujillo ME, Suzuki K, Ludwig W, Whitman WB (2012) Bergey’s manual of systematic bacteriology Vol. Five, Second.; London.

Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: Molecular Evolutionary Genetics Analysis Version 6.0. Mol Biol Evol 30(12):2725–2729. https://doi.org/10.1093/molbev/mst197

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(4):809–819. https://doi.org/10.1007/s10482-012-9863-3

Powers EM (1995) Efficacy of the Ryu nonstaining KOH technique for rapidly determining gram reactions of food-borne and waterborne bacteria and yeasts. Appl Environ Microbiol 61(10):3756–3758

Kokare CR, Mahadik KR, Kadam SS, Chopade BA (2004) Isolation of bioactive marine actinomycetes from sediments isolated from Goa and Maharashtra Coastlines (West Coast of India) 33(September):248–256

Duncan K, Haltli B, Gill K a, Kerr RG (2014) Bioprospecting from marine sediments of New Brunswick, Canada: exploring the relationship between total bacterial diversity and Actinobacteria diversity. Mar Drugs 12(2):899–925. https://doi.org/10.3390/md12020899

Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski R a, Oakley BB, Parks DH, Robinson CJ, Sahl JW, Stres B, Thallinger GG, Van Horn DJ, Weber CF (2009) Introducing Mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75(23):7537–7541. https://doi.org/10.1128/AEM.01541-09

Chao A, Chiu C-HSR (2016) Estimation and comparison. Wiley StatsRef: statistics reference online; John Wiley & Sons, Ltd: Chichester, UK, pp 1–26

Özcan K, Aksoy SÇ, Kalkan O, Uzel A, Hames-Kocabas EE, Bedir E (2013) Diversity and antibiotic-producing potential of cultivable marine-derived actinomycetes from coastal sediments of Turkey. J Soils Sediments 13(Wilkins 1996):1493–1501. https://doi.org/10.1007/s11368-013-0734-y

Jensen PR, Dwight R, Fenical W (1991) Distribution of actinomycetes in near-shore tropical marine sediments. Appl Environ Microbiol 57(4):1102–1108

Youssef NH, Couger MB, McCully AL, Criado AEG, Elshahed MS (2015) Assessing the global phylum level diversity within the bacterial domain: a review. J Adv Res 6:269–282

Floros DJ, Jensen PR, Dorrestein PC, Koyama N (2016) A metabolomics guided exploration of marine natural product chemical space. Metabolomics 12

Prieto-Davó, a; Fenical, W.; Jensen, P. Comparative actinomycete diversity in marine sediments. Aquat Microb Ecol 2008, 52 (July), 1–11 DOI: https://doi.org/10.3354/ame01211.

Jensen PR, Williams PG, Oh D-C, Zeigler L, Fenical W (2007) Species-specific secondary metabolite production in marine actinomycetes of the genus Salinispora. Appl Environ Microbiol 73(4):1146–1152. https://doi.org/10.1128/AEM.01891-06

Aranda-Cirerol N (2002) Water quality and sustainable development in Yucatán Peninsula. Environ. Res. J, 5 (6).

Herrera-Silveira JA, Morales-ojeda SM (2009) Evaluation of the health status of a coastal ecosystem in Southeast Mexico: assessment of water quality, phytoplankton and submerged aquatic vegetation. Mar Pollut Bull 59(1–3):72–86. https://doi.org/10.1016/j.marpolbul.2008.11.017

Valdes DS, Real E (1998) Variations and relationships of salinity, nutrients and suspended solids in Chelem coastal lagoon at Yucatan, Mexico. Indian J Mar Sci 27(2):149–156

Rashad FM, Fathy HM, El-zayat AS, Elghonaimy AM (2015) Isolation and characterization of multifunctional Streptomyces species with antimicrobial, nematicidal and phytohormone activities from marine environments in Egypt. 175:34–47.

Tian X, Zhang Z, Yang T, Chen M, Li J, Chen F, Yang J, Li W, Zhang B, Zhang Z, Wu J, Zhang C, Long L, Xiao J (2016) Comparative genomics analysis of Streptomyces species reveals their adaptation to the marine environment and their diversity at the genomic level. Front Microbiol 7:998. https://doi.org/10.3389/fmicb.2016.00998

Fan L, Liu Y, Li Z, Baumann HI, Kleinschmidt K, Ye W, Imhoff JF, Kleine M, Cai D (2011) Draft genome sequence of the marine Streptomyces sp. strain PP-C42, isolated from the Baltic Sea. J Bacteriol 193(14):3691–3692. https://doi.org/10.1128/JB.05097-11

Leipoldt F, Zeyhle P, Kulik A, Kalinowski J, Heide L, Kaysser L (2015) Diversity of ABBA prenyltransferases in marine Streptomyces sp. CNQ-509: promiscuous enzymes for the biosynthesis of mixed terpenoid compounds. PLoS One 10(12):e0143237. https://doi.org/10.1371/journal.pone.0143237

Feling RH, Buchanan GO, Mincer TJ, Kauffman CA, Jensen PR, Fenical W (2003) Salinosporamide A: a highly cytotoxic proteasome inhibitor from a novel microbial source, a marine bacterium of the new genus Salinospora. Angew Chem Int Ed 42(3):355–357. https://doi.org/10.1002/anie.200390115

Tian XP, Long LJ, Wang FZ, Xu Y, Li J, Zhang J, Zhang CS, Zhang S, Li WJ (2012) Streptomyces nanhaiensis sp. Nov., a marine streptomycete isolated from a deep-sea sediment. Int J Syst Evol Microbiol 62(4):864–868. https://doi.org/10.1099/ijs.0.031591-0

Murray G (2007) Constructing paradise: the impacts of big tourism in the Mexican coastal zone. Coast Manag 35(2–3):339–355. https://doi.org/10.1080/08920750601169600

Fenchel T, Finlay BJ (2004) The ubiquity of small species: patterns of local and global diversity. Bioscience 54(8):777. https://doi.org/10.1641/0006-3568(2004)054[0777:TUOSSP]2.0.CO;2

R Core Team. R: a language and environment for statistical computing; 2015; Vol. 1.

Rahalison L, Hamburger M, Hostettmann K, Monod M, Frenk E (1991) A bioautographic agar overlay method for the detection of antifungal compounds from higher plants. Phytochem Anal 2(5):199–203. https://doi.org/10.1002/pca.2800020503

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Microbial Ecology

Tập 77

839-851

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