Abstract
The biodiversity of actinobacteria in the Mediterranean Sea habitat has drawn limited attention compared to that paid to terrestrial habitats. The work presented here focused on the biodiversity of culturable marine actinobacteria from sediments and seawater collected from the Algerian coast, and led to the identification of 114 actinobacterial isolates. The morphological study revealed higher actinobacterial diversity in sediment than in seawater. Fifty strains were selected for 16 S rRNAgene sequencing. The results revealed that the isolates belonged to ten different genera, Streptomyces (n = 17) and Micromonospora (n = 15) being the most dominant. The remaining actinobacterial isolates, identified as belonging to rare genera, included Nocardia (n = 5), Nocardiopsis (n = 3), Saccharothrix (n = 2), Rhodococcus (n = 2), Promicromonospora (n = 2), Nonomuraea (n = 2), Actinomadura (n = 1) and Saccharomonospora (n = 1). Interestingly, through 16 S rRNA sequence-based identification and phylogenetic analysis, two strains of the genus Streptomyces (MAT1 and MAS22) and a strain of the genus Nonomuraea (MAG8) both constituted a novel species. Screening of antibacterial activity of identified isolates against a panel of human pathogenic bacteria demonstrated that 36% of the isolates were active, particularly against Gram-positive bacteria. The ability to grow in the presence of NaCl and seawater revealed that 98% of the strains were halotolerant, with different levels of NaCl acceptance (from 3 to 13%) but no isolates required seawater to grow.
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Data Availability
The DNA sequences were deposited in the National Centre for Biotechnology Information (NCBI)-GenBank under accession numbers from OM033412 to OM033461.
Abbreviations
- CA:
-
Cluster Analysis
- ISCC-NBS:
-
Inter-Society Color Council-National Bureau of Standards
- MEGA:
-
Molecular Evolutionary Genetics Analysis
- NCBI:
-
National Centre for Biotechnology Information
- PCA:
-
Principal Component Analysis
- PCR:
-
Polymerase Chain Reaction
References
Abdelfattah MS, Elmallah MIY, Hawas UW, Eid MAG (2016) Isolation and characterization of marine-derived actinomycetes with cytotoxic activity from the Red Sea coast. Asian Pac J Trop Biomed 6:651–657. https://doi.org/10.1016/j.apjtb.2016.06.004
Aghighi S, Shahidi Bonjar GH, Rawashdeh R, Batayneh S, Saadoun I (2004) First report of antifungal spectra of activity of Iranian actinomycetes strains against Alternaria solani, Alternaria alternate, Fusarium solani, Phytophthora megasperma, Verticillium dahliae and Saccharomyces cerevisiae. Asian J Plant Sci 33:463–471. https://doi.org/10.3923/ajps.2004.463.471
Ait Barka E, Vatsa P, Sanchez L, Gaveau-Vaillant N, Jacquard C, Klenk HP, Clément C, Ouhdouch Y, van Wezel GP (2016) Taxonomy, physiology, and natural products of Actinobacteria. Microbiol Mol Biol Rev 80:1–43. https://doi.org/10.1128/MMBR.00019-15
Arumugam T, Kumar PS, Kameshwar R, Prapanchana K (2017) Screening of novel actinobacteria and characterization of the potential isolates from mangrove sediment of south coastal India. Microb Pathog 107:225–233. https://doi.org/10.1016/j.micpath.2017.03.035
Azman A-S, Othman I, Velu S, Chan S, Lee KG LH (2015) Mangrove rare actinobacteria: taxonomy, natural compound, and discovery of bioactivity. Front Microbiol 6:856. https://doi.org/10.3389/fmicb.2015.00856
Ballav S, Kerkar S, Thomas S, Augustine N (2015) Halophilic and halotolerant actinomycetes from a marine saltern of Goa, India producing anti-bacterial metabolites. J Biosci Bioeng 119:323–330. https://doi.org/10.1016/j.jbiosc.2014.08.017
Becerril-Espinosa A, Guerra-Rivas G, Ayala-Sánchez N, Soria-Mercado IE (2012) Antitumor activity of Actinobacteria isolated in marine sediment from Todos Santos Bay, Baja California, Mexico. Rev Biol Mar oceanogr 47:317–325. https://doi.org/10.4067/S0718-19572012000200013
Bredholdt H, Galatenko OA, Engelhardt K, Fjærvik E, Terekhova LP, Zotchev SB (2007) Rare actinomycete bacteria from the shallow water sediments of the Trondheim fjord, Norway: isolation, diversity and biological activity. Environ Microbiol 9:2756–2764. https://doi.org/10.1111/j.1462-2920.2007.01387.x
Bredholt H, Fjærvik E, Johnsen G, Zotchev SB (2008) Actinomycetes from sediments in the Trondheim Fjord, Norway: Diversity and Biological Activity. Mar Drugs 6:12–24. https://doi.org/10.3390/md6010012
Bérdy J (2012) Thoughts and facts about antibiotics: where we are now and where we are heading. J. Antibiot 65, 385–395. https://doi.org/10.1038/ja.2012.27
Chen P, Zhang L, Guo X, Dai X, Liu L, Xi L, Wang J, Song L, Wang Y, Zhu Y, Huang L, Huang Y (2016) Diversity, biogeography, and biodegradation potential of actinobacteria in the deep-sea sediments along the southwest indian ridge. Front Microbiol 7:1340. https://doi.org/10.3389/fmicb.2016.01340
Claverías FP, Undabarrena AN, González M, Seeger M, Cámara BP (2015) Culturable diversity and antimicrobial activity of Actinobacteria from marine sediments in Valparaíso bay, Chile. Front Microbiol 6:737. https://doi.org/10.3389/fmicb.2015.00737
Cumsille A, Undabarrena A, González V, Claverías F, Rojas C, Cámara B (2017) Biodiversity of Actinobacteria from the south pacific and the assessment of Streptomyces chemical diversity with metabolic profiling. Mar Drugs 15:286. https://doi.org/10.3390/md15090286
Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791. https://doi.org/10.1111/j.1558-5646.1985.tb00420.x
Gärtner A, Blümel M, Wiese J, Imhoff JF (2011) Isolation and characterisation of bacteria from the Eastern Mediterranean deep sea. Antonie Van Leeuwenhoek 100:421–435. https://doi.org/10.1007/s10482-011-9599-5
Hakvåg S, Fjærvik E, Josefsen KD, Ian E, Ellingsen TE, Zotchev SB (2008) Characterization of Streptomyces spp. isolated from the sea surface microlayer in the Trondheim Fjord, Norway. Mar Drugs 6:620–635. https://doi.org/10.3390/md6040620
Hong K, Gao A-H, Xie Q-Y, Gao HG, Zhuang L, Lin HP, Yu HP, Li J, Yao XS, Goodfellow M, Ruan JS (2009) Actinomycetes for marine drug discovery isolated from mangrove soils and plants in China. Mar Drugs 7:24–44. https://doi.org/10.3390/md7010024
Hsu SC, Lockwood JL (1975) Powdered chitin agar as a selective medium for enumeration of actinomycetes in water and soil. Appl Microbiol 29:422–426. https://doi.org/10.1128/am.29.3.422-426.1975
Imada C, Koseki N, Kamata M, Kobayashi T, Hamada-Sato N (2007) Isolation and characterization of antibacterial substances produced by marine actinomycetes in the presence of seawater. Actinomycetologica 21:27–31. https://doi.org/10.3209/saj.SAJ210104
Imada C, Masuda S, Kobayashi T, Hamada-Sato N, Nakashima T (2010) Isolation and characterization of marine and terrestrial actinomycetes using a medium supplemented with NaCl. Actinomycetologica 24:12–17. https://doi.org/10.3209/saj.SAJ240104
Jose PA, Jha B (2017) Intertidal marine sediment harbours Actinobacteria with promising bioactive and biosynthetic potential. Sci Rep 7:10041. https://doi.org/10.1038/s41598-017-09672-6
Kim M, Oh HS, Park SC, Chun J (2014) Towards a taxonomic coherence between average nucleotide identity and 16S rRNA gene sequence similarity for species demarcation of prokaryotes. Int J Syst Evol Microbiol 64:346–351. https://doi.org/10.1099/ijs.0.059774-0
Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120. https://doi.org/10.1007/BF01731581
Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874. https://doi.org/10.1093/molbev/msw054
Laassami A, Yekkour A, Meklat A, Djemouai N, Zitouni A, Mokrane S, Lecomte P, Rey P, Berraf-Tebbal A (2020) Actinobacteria associated with vineyard soils of algeria: classification, antifungal potential against grapevine trunk pathogens and plant growth-promoting features. Curr Microbiol 77:2831–2840. https://doi.org/10.1007/s00284-020-02097-x
Lê S, Josse J, Husson F (2008) FactoMineR: an R Package for Multivariate Analysis. J Stat Softw 25:1–18. https://doi.org/10.18637/jss.v025.i018
Lee LH, Zainal N, Azman A-S, Eng SK, Goh BH, Yin WF, Ab Mutalib NS, Chan KG (2014) Diversity and antimicrobial activities of actinobacteria isolated from tropical mangrove sediments in Malaysia. Sci World J e698178. https://doi.org/10.1155/2014/698178
Legendre P, Legendre L (1998) Numerical Ecology, Second English edition. Elsevier Science, Amsterdam, p 852
Liu B, Li J, Chen M, Hao X, Cao F, Tan Y, Ping Y, Wang Y, Xiao C, Gan M (2018) Seco-Tetracenomycins from the marine-derived actinomycete Saccharothrix sp. Mar Drugs 16:10–10. https://doi.org/10.3390/md16100345
Liu D, Coloe S, Baird R, Pedersen J (2000) Rapid mini-preparation of fungal DNA for PCR. J Clin Microbiol 38:471–471. https://doi.org/10.1128/JCM.38.1.471-471.2000
Maldonado LA, Fenical W, Jensen PR, Kauffman CA, Mincer TJ, Ward AC, Bull AT, Goodfellow M (2005a) 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
Maldonado LA, Fragoso-Yáñez D, Pérez-García A, Rosellón-Druker J, Quintana ET (2009) Actinobacterial diversity from marine sediments collected in Mexico. Antonie Van Leeuwenhoek 95:111–120. https://doi.org/10.1007/s10482-008-9294-3
Maldonado LA, Stach JEM, Pathom-aree W, Ward AC, Bull AT, Goodfellow M (2005b) Diversity of cultivable actinobacteria in geographically widespread marine sediments. Antonie Van Leeuwenhoek 87:11–18. https://doi.org/10.1007/s10482-004-6525-0
Meena B, Anburajan L, Vinithkumar NV, Kirubagaran R, Dharani G (2019) Biodiversity and antibacterial potential of cultivable halophilic actinobacteria from the deep sea sediments of active volcanic Barren Island. Microb Pathog 132:129–136. https://doi.org/10.1016/j.micpath.2019.04.043
Mincer TJ, Jensen PR, Kauffman CA, Fenical W (2002) Widespread and persistent populations of a major new marine actinomycete taxon in ocean sediments. Appl Environ Microbiolo 68:5005–5011. https://doi.org/10.1128/AEM.68.10.5005-5011.2002
Okazaki T, Okami Y (1975) Actinomycetes tolerant to increased NaCl concentration and their metabolites. J Ferment Technolo 53:833–840
Ouchari L, Boukeskasse A, Bouizgarne B, Ouhdouch Y (2019) Antimicrobial potential of actinomycetes isolated from the unexplored hot Merzouga desert and their taxonomic diversity. Biol Open 8:bio035410. https://doi.org/10.1242/bio.035410
Pawlowski K, Demchenko KN (2012) The diversity of actinorhizal symbiosis. Protoplasma 249:967–979. https://doi.org/10.1007/s00709-012-0388-4
Petro C, Zäncker B, Starnawski P, Jochum LM, Ferdelman TG, Jørgensen BB, Røy Hans, Kjeldsen KU, Schramm A (2019) Marine deep biosphere microbial communities assemble in near-surface sediments in Aarhus Bay. Front Microbiol 10:758. https://doi.org/10.3389/fmicb.2019.00758
Prieto-Davó A, Dias T, Gomes SE, Rodrigues S, Parera-Valadez Y, Borralho PM, Pereira F, Rodrigues CMP, Santos-Sanches I, Gaudêncio SP (2016) The madeira archipelago as a significant source of marine-derived actinomycete diversity with anticancer and antimicrobial potential. Front Microbiol 7:1594. https://doi.org/10.3389/fmicb.2016.01594
Prieto-Davó A, Fenical W, Jensen PR (2008) Comparative actinomycete diversity in marine sediments. Aquat Microb Ecol 52:1–11. https://doi.org/10.3354/ame01211
Ramesh S, Mathivanan N (2009) Screening of marine actinomycetes isolated from the Bay of Bengal, India for antimicrobial activity and industrial enzymes. World J Microbiol Biotechnol 25:2103–2111. https://doi.org/10.1007/s11274-009-0113-4
Ribeiro I, Girão M, Alexandrino DAM, Ribeiro T, Santos C, Pereira F, Mucha AP, Urbatzka R, Leão PN, Carvalho MF (2020) Diversity and bioactive potential of actinobacteria isolated from a coastal marine sediment in Northern Portugal. Microorganisms 8:1691. https://doi.org/10.3390/microorganisms8111691
Rodrigues RR, Pineda RP, Barney JN, Nilsen ET, Barrett JE, Williams MA (2015) Plant invasions associated with change in root-zone microbial community structure and diversity. PLoS ONE 10:e0141424. https://doi.org/10.1371/journal.pone.0141424
Sabido EM, Tenebro CP, Trono DJVL, Vicera CVB, Leonida SFL, Maybay JJWB, Reyes-Salarda R, Amago DS, Aguadera AMV, Octaviano MC, Saludes JP, Dalisay DS (2021) Insights into the variation in bioactivities of closely related Streptomyces strains from marine sediments of the Visayan sea against ESKAPE and ovarian cancer. Mar Drugs 19:441. https://doi.org/10.3390/md19080441
Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425. https://doi.org/10.1093/oxfordjournals.molbev.a040454
Sharma S, Fulke AB, Chaubey A (2019) Bioprospection of marine actinomycetes: recent advances, challenges and future perspectives. Acta Oceanol Sin 38:1–17. https://doi.org/10.1007/s13131-018-1340-z
Shirling EB, Gottlieb DY (1966) Methods for characterization of Streptomyces species1. Int J Syst Evol Microbiol 16(3):313–340. https://doi.org/10.1099/00207713-16-3-313
Siddharth S, Rai VR (2019) Isolation and characterization of bioactive compounds with antibacterial, antioxidant and enzyme inhibitory activities from marine-derived rare actinobacteria, Nocardiopsis sp. SCA21. Microb Pathog 137:103775. https://doi.org/10.1016/j.micpath.2019.103775
Subramani R, Aalbersberg W (2013) Culturable rare actinomycetes: diversity, isolation and marine natural product discovery. Appl Microbiol Biotechnol 97:9291–9321. https://doi.org/10.1007/s00253-013-5229-7
Subramani R, Sipkema D (2019) Marine rare actinomycetes: a promising source of structurally diverse and unique novel natural products. Mar Drugs 17:249. https://doi.org/10.3390/md17050249
Thawai C, Kudo T (2012) Promicromonospora thailandica sp. nov., isolated from marine sediment. Int J Syst Evol Microbiol 62:2140–2144. https://doi.org/10.1099/ijs.0.035972-0
Tuncer I, Bizsel N (2017) Phylogeny and physiology of actinomycetes and biogeochemical parameters in sediments of Eastern Mediterranean Sea. Int J Environ Sci Deve 8:581–585. https://doi.org/10.18178/ijesd.2017.8.8.1019
Vijayakumar R, Panneerselvam K, Muthukumar C, Thajuddin N, Panneerselvam A, Saravanamuthu R (2012) Optimization of antimicrobial production by a marine actinomycete Streptomyces afghaniensis VPTS3-1 isolated from palk strait, east coast of India. Indian J Microbiol 52:230–239. https://doi.org/10.1007/s12088-011-0138-x
Yekkour A, Bouras N, Smaoui S, Mellouli L, Barakate M (2021) Actinobacterial secondary metabolites from Maghrebian Ecosystems: an overview of half-century of investigation. In: Singh RP, Manchanda G, Bhattacharjee K, Panosyan H (eds) Microbes in Microbial Communities. Springer, Singapore. https://doi.org/10.1007/978-981-16-5617-0_2
Yoon S-H, Ha S-M, Kwon S, Lim J, Kim Y, Seo H, Chun J (2017) Introducing EzBioCloud: a taxonomically united database of 16S rRNA gene sequences and whole-genome assemblies. Int J Syst Evol Microbiol 67:1613–1617. https://doi.org/10.1099/ijsem.0.001755
Yu J, Zhang L, Liu Q, Qi X, Ji Y, Kim BS (2015) Isolation and characterization of actinobacteria from Yalujiang coastal wetland, North China. Asian Pac J Trop Biomed 5:555–560. https://doi.org/10.1016/j.apjtb.2015.04.007
Yuan M, Yu Y, Li HR, Dong N, Zhang XH (2014) Phylogenetic diversity and biological activity of actinobacteria isolated from the Chukchi Shelf marine sediments in the Arctic Ocean. Mar Drugs 12:1281–1297. https://doi.org/10.3390/md12031281
Zhang G, Cao T, Ying J, Yang Y, Ma L (2014) Diversity and novelty of actinobacteria in Arctic marine sediments. Antonie Van Leeuwenhoek 105:743–754. https://doi.org/10.1007/s10482-014-0130-7
Zhang L, Xi L, Ruan J, Huang Y (2012) Microbacterium marinum sp. nov., isolated from deep-sea water. Syst Appl Microbiol 35:81–85. https://doi.org/10.1016/j.syapm.2011.11.004
Zhang J, Sun QL, Zeng ZG, Chen S, Sun L (2015) Microbial diversity in the deep-sea sediments of Iheya North and Iheya Ridge, Okinawa Trough. Microbiol Res 177:43–52. https://doi.org/10.1016/j.micres.2015.05.006
Acknowledgements
We thank the late Prof. Sabaou N (LBSM, Ecole Normale Supérieure de Kouba, Algiers, Algeria) for great help in isolation and taxonomic analysis of actinobacteria.
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This research was supported by the Laboratoire de Biologie des Systèmes Microbiens.
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A.M. performance of the experiments, and wrote the first draft of the manuscript, A.Y. supervision of the experiments, multivariate data analysis, discussion of the results and correction of the manuscript, M.Y.B. assistance in the evaluation the bioactivity test, N.B. technical assistance in actinobacterial characterization, A.Z. and S.M. secured funding and assistance in phylogenitic study, A.M. designed and planned the experiments with correction of the manuscript, and C.V.V. finance of the molecular identification, technical assistance in molecular identification and correction of the manuscript.
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Matmoura, A., Yekkour, A., Boufadi, M.Y. et al. Exploration of actinobacteria communities in seawater and sediments of mediterranean basin from Algerian coast displays hight diversity with new taxa and antibacterial potential. Biologia 78, 2219–2231 (2023). https://doi.org/10.1007/s11756-023-01353-2
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DOI: https://doi.org/10.1007/s11756-023-01353-2