Biosynthetic and antimicrobial potential of actinobacteria isolated from bulrush rhizospheres habitat in Zhalong Wetland, China

Li, Yamei; Li, Yumei; Li, Qiang; Gao, Juan; Wang, Juanjuan; Luo, Yan; Fan, Xiangyu; Gu, Pengfei

doi:10.1007/s00203-018-1474-6

Original Paper
Published: 24 January 2018

Biosynthetic and antimicrobial potential of actinobacteria isolated from bulrush rhizospheres habitat in Zhalong Wetland, China

Yamei Li¹,
Yumei Li¹,
Qiang Li¹,
Juan Gao¹,
Juanjuan Wang¹,
Yan Luo¹,
Xiangyu Fan¹ &
Pengfei Gu¹

Archives of Microbiology volume 200, pages 695–705 (2018)Cite this article

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Abstract

The wetland ecosystem is known to possess unique vegetation and serves multiple functions within the environment. In this study, bacterial bioprospecting of bulrush rhizospheres in the Zhalong Wetland, China, was performed using comprehensive methods, including strain isolation and phylogenetic analysis, PCR detection of biosynthetic gene clusters, assessment of antimicrobial activity, metabolite profiling and genome analysis. A total of 27 actinobacterial strains were isolated, and their biosynthetic gene clusters (NRPS, PKS-I and PKS-II) were investigated; all of the tested strains had at least one of the three aforementioned biosynthetic gene clusters. Furthermore, fermentation broth extracts produced by these strains showed antimicrobial activities against certain pathogens, and ten of the extracts exhibited broad-spectrum antimicrobial activity. Liquid chromatography–mass spectrometry (LC–MS) analysis indicated chemical diversity of secondary metabolites from these extracts. Among these strains, ZLSD-24 generated the largest amounts and types of secondary metabolites. Subsequent genome analysis showed that 41 secondary metabolite biosynthetic gene clusters were present in the strain ZLSD-24, which was in accordance with the LC–MS data. Taken together, the results of this study reveal that bulrush rhizosphere habitat in the Zhalong wetland is a promising source of novel natural products.

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References

Butler S (2010) Macquarie concise dictionary, 5th edn. Macquarie Dictionary Publishers Ltd, Sydney
Google Scholar
Chen Y, Yin M, Horsman GP et al (2011) Improvement of the enediyne antitumor antibiotic C-1027 production by manipulating its biosynthetic pathway regulation in Streptomyces globisporus. J Nat Prod 74:420–424. https://doi.org/10.1021/np100825y
Article PubMed PubMed Central CAS Google Scholar
Cheng C, MacIntyre L, Abdelmohsen UR et al (2015) Biodiversity, anti-trypanosomal activity screening, and metabolomic profiling of actinomycetes isolated from Mediterranean sponges. PLoS One 10:e0138528. https://doi.org/10.1371/journal.pone.0138528
Article PubMed PubMed Central CAS Google Scholar
Claverías FP, Undabarrena A, González M et al (2015) Culturable diversity and antimicrobial activity of Actinobacteria from marine sediments in Valparaíso bay, Chile. Front Microbiol 6:737–747. https://doi.org/10.3389/fmicb.2015.00737
Article PubMed PubMed Central Google Scholar
Deng MR, Guo J, Ma LY et al (2015) Complete genome sequence of Streptomyces vietnamensis GIMV4.0001 T, a genetically manipulable producer of the benzoisochromanequinone antibiotic granaticin. J Biotechnol 200:6–7. https://doi.org/10.1016/j.jbiotec.2015.02.009
Article PubMed CAS Google Scholar
Denny P (1994) Biodiversity and wetlands. Wet Ecol Manag 3:55–61
Article Google Scholar
Garrido LM, Lombó F, Baig I et al (2006) Insights in the glycosylation steps during biosynthesis of the antitumor anthracycline cosmomycin: characterization of two glycosyltransferase genes. Appl Microbiol Biotechnol 73:122–131. https://doi.org/10.1007/s00253-006-0453-z
Article PubMed PubMed Central CAS Google Scholar
Hong JS, Park SH, Choi CY et al (2004) New olivosyl derivatives of methymycin/pikromycin from an engineered strain of Streptomyces venezuelae. FEMS Microbiol Lett 238:391–399. https://doi.org/10.1016/j.femsle.2004.08.00
PubMed CAS Article Google Scholar
Hugo WB, Russell AD (1983) Pharmaceutical microbiology, 3rd edn. Blackwell, Oxford
Google Scholar
Jin H, Yang XY, Yan ZQ et al (2014) Characterization of rhizosphere and endophytic bacterial communities from leaves, stems and roots of medicinal Stellera chamaejasme L. Syst Appl Microbiol 37:376–385. https://doi.org/10.1016/j.syapm.2014.05.001
Article PubMed Google Scholar
Khamma S, Yokata A, Lumyong S (2009) Actinomycetes isolated from medicinal plant rhizospheric soils: diversity and screening of antifungal compounds, indole-3-acetic acid and siderophore production. World J Microbiol Biotechnol 25:649–655. https://doi.org/10.1007/s11274-008-9933-x
Article CAS Google Scholar
Kim ES, Song JY, Kim DW et al (2008) Involvement of beta-lactamase inhibitory protein, BLIP-II, in morphological differentiation of Streptomyces exfoliatus SMF19. J Microbiol Biotechnol 18:1884–1891. https://doi.org/10.4014/jmb.0800.203
PubMed CAS Article Google Scholar
Lee LH, Zainal N, Azman AS et al (2014) Diversity and antimicrobial activities of actinobacteria isolated from tropical mangrove sediments in Malaysia. Sci World J 2014:698178–698178. https://doi.org/10.1155/2014/698178
Article Google Scholar
Li HY, Zhang GX, Li XQ (2012) Spatial characteristics of water quality of wetland in Northeast China—the case of Zhalong Wetland. Proced Environ Sci 12:1024–1029. https://doi.org/10.1016/j.proenv.2012.01.382
Article CAS Google Scholar
Li J, Dong JD, Yang J et al (2014) Detection of polyketide synthase and nonribosomal peptide synthetase biosynthetic genes from antimicrobial coral-associated actinomycetes. Antonie Van Leeuwenhoek 106:623–635. https://doi.org/10.1007/s10482-014-0233-1
Article PubMed CAS Google Scholar
Matter AM, Hoot SB, Anderson PD et al (2009) Valinomycin biosynthetic gene cluster in Streptomyces: conservation, ecology and evolution. PLoS One 4:e7194. https://doi.org/10.1371/journal.pone.0007194
Article PubMed PubMed Central CAS Google Scholar
Mendes R, Garbeva P, Raaijmaker JM (2013) The rhizosphere microbiome: significance of plant beneficial, plant pathogenic, and human pathogenic microorganisms. FEMS Microbiol Rev 37:634–663. https://doi.org/10.1111/1574-6976.12028
Article PubMed CAS Google Scholar
Miao V, Davies J (2010) Actinobacteria: the good, the bad, and the ugly. Anton Leeuw 98:143–150. https://doi.org/10.1007/s10482-010-9440-6
Article Google Scholar
Myronovskyi M, Tokovenko B, Manderscheid N et al (2013) Complete genome sequence of Streptomyces fulvissimus. J Biotechnol 168:117–118. https://doi.org/10.1016/j.jbiotec.2013.08.013
Article PubMed CAS Google Scholar
Nimaichand S, Devi AM, Tamreihao K et al (2015) Actinobacterial diversity in limestone deposit sites in Hundung, Manipur (India) and their antimicrobial activities. Front Microbiol 6:413–422. https://doi.org/10.3389/fmicb.2015.00413
Article PubMed PubMed Central Google Scholar
Pascual J, Blanco S, García-López M et al (2016) Assessing bacterial diversity in the rhizosphere of Thymus zygis growing in the Sierra Nevada National Park (Spain) through culture-dependent and independent approaches. PLoS One 11:e0146558. https://doi.org/10.1371/journal.pone.0146558
Article PubMed PubMed Central Google Scholar
Philippot L, Raaijmaker JM, Lemanceau P et al (2013) Going back to the roots: the microbial ecology of the rhizosphere. Nat Rev Microbiol 11:789–799. https://doi.org/10.1038/nrmicro3109
Article PubMed CAS Google Scholar
Richard JLM, Gilbert S (2006) Chitin in a dual role as substrate for Streptomyces griseus and as adsorbent for streptomycin produced during fermentation. Enzym Microbial Technol 38:657–664. https://doi.org/10.1016/j.enzmictec.2005.07.017
Article CAS Google Scholar
Sanghvi GV, Ghevariya D, Gosai S et al (2014) Isolation and partial purification of erythromycin from alkaliphilic Streptomyces werraensis isolated from Rajkot, India. Biotechnol Rep (Amst) 1–2:2–7. https://doi.org/10.1016/j.btre.2014.05.003
Article Google Scholar
Schorn MA, Alanjary MM, Aguinaldo K, Korobeynikov A, Podell S, Patin N, Lincecum T, Jensen PR, Ziemert N, Moore BS (2016) Sequencing rare marine actinomycete genomes reveals high density of unique natural product biosynthetic gene clusters. Microbiology 162(12):2075–2086. https://doi.org/10.1099/mic.0.000386
Article PubMed PubMed Central CAS Google Scholar
Schwarzer D, Marahiel MA (2001) Multimodular biocatalysts for natural product assembly. Naturwissenschaften 88:93–101. https://doi.org/10.1007/s001140100211
Article PubMed CAS Google Scholar
Sun W, Zhang F, He L et al (2015) Actinomycetes from the South China Sea sponges: isolation, diversity, and potential for aromatic polyketides discovery. Front Microbiol 6:1048–1062. https://doi.org/10.3389/fmicb.2015.01048
PubMed PubMed Central Article Google Scholar
Takahashi YO, Omura S et al (2003) Isolation of new actinomycete strains for the screening of new bioactive compounds. J Gen Appl Microbiol 49:141–154. https://doi.org/10.2323/jgam.49.141
Article PubMed CAS Google Scholar
Torres-Cortés G, Millán V, Fernández-González J et al (2012) Bacterial community in the rhizosphere of the cactus species Mammillaria carnea during dry and rainy seasons assessed by deep sequencing. Plant Soil 357:275–288. https://doi.org/10.1007/s11104-012-1152-4
Article CAS Google Scholar
Umeama H, Takeuchi T, Nitta K et al (1953) Studies on anti-tumor substances produced by microorganisms. III. On sarkomycin produced by a strain resembling to Streptomyces erythrochromogenes. J Antibiot (Tokyo) 6:147–152
Google Scholar
Walsh CT (2008) The chemical versatility of natural-product assembly lines. Acc Chem Res 41:4–10. https://doi.org/10.1021/ar7000414
Article PubMed CAS Google Scholar
Wang ZQ, Fu JC, Hao CY et al (2009) The spatial–temporal pattern changes of the red crowned crane (Grus japonensis) population in Zhalong NNR and the related driving forces. Acta Ecol Sin 29:351–356. https://doi.org/10.1016/j.chnaes.2009.09.016
Article CAS Google Scholar
Wang Y, Chen Y, Shen Q et al (2011) Molecular cloning and identification of the laspartomycin biosynthetic gene cluster from Streptomyces viridochromogenes. Gene 483:11–21. https://doi.org/10.1016/j.gene.2011.05.005
Article PubMed PubMed Central CAS Google Scholar
Wang X, Tabudravu J, Rateb ME et al (2013) Identification and characterization of the actinomycin G gene cluster in Streptomyces iakyrus. Molecul Biosyst 9:1286–1289. https://doi.org/10.1039/c3mb70081j
Article CAS Google Scholar
You YH, Park JM, Park JH et al (2015) Diversity of endophytic fungi associated with the roots of four aquatic plants inhabiting two wetlands in Korea. Mycobiology 43:231–238. https://doi.org/10.5941/MYCO.2015.43.3.231
Article PubMed PubMed Central Google Scholar
Yu D, Xu F, Zeng J et al (2012) Type III polyketide synthases in natural product biosynthesis. IUBMB Life 64:285–295. https://doi.org/10.1002/iub.1005
Article PubMed CAS Google Scholar

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Acknowledgements

Thanks to a Project of Shandong Province Higher Educational Science and Technology Program (YE13), Primary Research and Development Plan of Shandong Province (2016GSF121018).

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School of Biological Science and Biotechnology, University of Jinan, Jinan, China
Yamei Li, Yumei Li, Qiang Li, Juan Gao, Juanjuan Wang, Yan Luo, Xiangyu Fan & Pengfei Gu

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Yamei Li
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Yumei Li
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Qiang Li
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Juan Gao
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Juanjuan Wang
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Yan Luo
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Xiangyu Fan
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Pengfei Gu
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Correspondence to Yumei Li.

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Communicated by Shuang-Jiang Liu.

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Li, Y., Li, Y., Li, Q. et al. Biosynthetic and antimicrobial potential of actinobacteria isolated from bulrush rhizospheres habitat in Zhalong Wetland, China. Arch Microbiol 200, 695–705 (2018). https://doi.org/10.1007/s00203-018-1474-6

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Received: 13 April 2017
Revised: 06 November 2017
Accepted: 03 January 2018
Published: 24 January 2018
Issue Date: July 2018
DOI: https://doi.org/10.1007/s00203-018-1474-6

Keywords

Actinobacteria
Wetland
Biosynthetic
Antimicrobial
Genome