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Genetic and Phenotypic Heterogeneity of the Nocardiopsis alba Strains of Seawater

Abstract

This study deals with the genetic and phenotypic heterogeneity of the marine Nocardiopsis alba strains isolated during pre-monsoon, monsoon and post-monsoon seasons. The isolates were characterized for their morphological and biochemical attributes, growth media preferences, antibiotic susceptibility and extracellular enzyme secretion. Nocardiopsis alba strains were assessed against 12 different antibiotics, and the responses were expressed in terms of the multiple antibiotic resistance (MAR) number. The majority of the strains produced multiple extracellular enzymes: proteases, amylases and lipases. Further, the strains were characterized on the basis of 16S rRNA gene sequencing and the majority were identified as Nocardiopsis alba along with few strains of Streptomyces lopnurensis, Nocardiopsis synnemataformans and Nocardiopsis dassonvillei. Neighbor-joining (NJ) phylogenetic tree suggested variation among the genetically similar Nocardiopsis alba species. The study establishes significant heterogeneity with respect to genetic and phenotypic characteristics of the strains of Nocardiopsis alba. Phylogenetic tree and phenogram-based comparison reflect the heterogeneity in terms of different clustering patterns of the strains. Further, the whole genome sequence data available in the literature also confirm the observed heterogeneity. Nocardiopsis alba strains displayed a relatively regressive pattern of dependence on the environmental factors based on the canonical correspondence analysis plot. The study represents cultivation, characterization, phylogenetic analysis and enzymatic potential of the Nocardiopsis alba species of seawater origin.

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References

  1. Caton TM, Witte LR, Ngyuen HD, Buchheim JA, Buchheim MA, Schneegurt MA (2004) Halotolerant aerobic heterotrophic bacteria from the Great Salt Plains of Oklahoma. Microb Ecol 48(4):449–462

    CAS  Article  Google Scholar 

  2. Mehetre G, Shah M, Dastager SG, Dharne MS (2018) Untapped bacterial diversity and metabolic potential within Unkeshwar hot springs India. Arch Microbiol. https://doi.org/10.1007/s00203-018-1484-4

    Article  PubMed  Google Scholar 

  3. Law JWF, Tan KX, Wong SH, Ab Mutalib NS, Lee LH (2018) Taxonomic and characterization methods of streptomyces: a review. Prog Microb Mol Biol. https://doi.org/10.36877/pmmb.a0000009

    Article  Google Scholar 

  4. Amin A, Ahmed I, Salam N, Kim BY, Singh D, Zhi XY, Xiao M, Li WJ (2017) Diversity and distribution of thermophilic bacteria in hot springs of Pakistan. Microb Ecol 74(1):116–127. https://doi.org/10.1007/s00248-017-0930-1

    Article  PubMed  Google Scholar 

  5. Pontes DS, Lima-Bittencourt CI, Azevedo MSP, Chartone-Souza E, Nascimento AMA (2007) Phenotypic and genetic analysis of Enterobacter spp. from a Brazilian oligotrophic freshwater lake. Can J Microbiol 53(8):983–991. https://doi.org/10.1139/W07-060

    CAS  Article  PubMed  Google Scholar 

  6. Mangamuri UK, Muvva V, Poda S, Kamma S (2012) Isolation, identification and molecular characterization of rare actinomycetes from mangrove ecosystem of Nizampatnam. Mal J Microbiol 8(2):83–91

    CAS  Google Scholar 

  7. Bhatt HB, Gohel SD, Singh SP (2018) Phylogeny, novel bacterial lineage and enzymatic potential of haloalkaliphilic bacteria from the saline coastal desert of Little Rann of Kutch, Gujarat, India. 3 Biotech 8(1):53. https://doi.org/10.1007/s13205-017-1075-0

    Article  PubMed  PubMed Central  Google Scholar 

  8. Sheikh M, Rathore D, Gohel S, Singh S (2018) Marine actinobacteria associated with the invertebrates hosts: a rich source of bioactive compounds: a review. JCTR 18(1)

  9. Rathore DS, Sheikh MA, Gohel SD, Singh SP (2019) Isolation strategies, abundance and characteristics of marine actinomycetes of Kachhighadi, Gujarat. India J Mar Biol Ass India 61(1):71–78. https://doi.org/10.6024/jmbai.2019.61.1.2028-11

    Article  Google Scholar 

  10. Gohel SD, Singh SP (2018) Molecular phylogeny and diversity of the salt-tolerant alkaliphilic actinobacteria inhabiting coastal Gujarat, India. Geomicrobiol J. https://doi.org/10.1080/01490451.2018.1471107

    Article  Google Scholar 

  11. Amsaveni R, Sureshkumar M, Vivekanandhan G, Bhuvaneshwari V, Kalaiselvi M, Padmalochana K, Preethikaharshini J (2015) Screening and isolation of pigment producing actinomycetes from soil samples. J Biosci Nanosci 2(2):24–28

    Google Scholar 

  12. APHA–American Public Health Association (2012) Standard methods for the examination of water and wastewater, 22nd edn. American Public Health Association, Washington, DC

    Google Scholar 

  13. Sheikh MA, Rathore DS, Gohel SD, Singh SP (2019) Cultivation and characteristics of the Marine Actinobacterial from the Sea water of Alang, Bhavnagar. Indian J Mar Sci 48(12):1896–1901

    Google Scholar 

  14. Bhatt HB, Singh SP (2020) Cloning, expression, and structural elucidation of a biotechnologically potential alkaline serine protease from a newly isolated Haloalkaliphilic Bacillus lehensis JO-26. Front Microbiol 11:941. https://doi.org/10.3389/fmicb.2020.00941

    Article  PubMed  PubMed Central  Google Scholar 

  15. Taddei A, Rodriguez MJ, Márquez-Vilchez E, Castelli C (2006) Isolation and identification of Streptomyces spp. from Venezuelan soils: morphological and biochemical studies. Microbiol Res 161(3):222–231. https://doi.org/10.1016/j.micres.2005.08.004

    CAS  Article  PubMed  Google Scholar 

  16. Greenacre M (2017) Correspondence analysis in practice. Chapman and Hall/CRC.

  17. 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 Pacific Asian Pac J Trop Biomed 5(7):555–560. https://doi.org/10.1016/j.apjtb.2015.04.007

    CAS  Article  Google Scholar 

  18. Bhatt HB, Singh SP (2016) Phylogenetic and phenogram based diversity of haloalkaliphilic bacteria from the saline desert. In: Bhukya B, Tangutur AD (eds) Microbial biotechnology: technological challenges and developmental trends. CRC Press, Boca Raton, pp 373–386

    Google Scholar 

  19. Buttigieg PL, Ramette A (2014) A guide to statistical analysis in microbial ecology: a community-focused, living review of multivariate data analyses. FEMS Microbiol Ecol 90(3):543–550. https://doi.org/10.1111/1574-6941.12437

    CAS  Article  PubMed  Google Scholar 

  20. TerBraak CJ (1986) Canonical correspondence analysis: a new eigenvector technique for multivariate direct gradient analysis. Ecology 67(5):1167–1179. https://doi.org/10.2307/1938672

    Article  Google Scholar 

  21. Tendler MD, Burkholder PR (1961) Studies on the thermophilic actinomycetes: i methods of cultivation. Appl Environ Microbiol 9(5):394–399

    CAS  Article  Google Scholar 

  22. Ackermann M (2015) A functional perspective on phenotypic heterogeneity in microorganisms. Nat Rev Microbiol 13(8):497–508. https://doi.org/10.1038/nrmicro3491

    CAS  Article  PubMed  Google Scholar 

  23. Jayabarath J, Musfira SA, Giridhar R, Arulmurugan R (2010) Biodegradation of carbofuran pesticide by saline soil actinomycetes. Int J Biotechnol Biochem 6(2):187–193

    Google Scholar 

  24. Albrecht R, Périssol C, Ruaudel F, Le Petit J, Terrom G (2010) Functional changes in culturable microbial communities during a co-composting process: carbon source utilization and co-metabolism. Waste Manage 30(5):764–770. https://doi.org/10.1016/j.wasman.2009.12.008Get

    CAS  Article  Google Scholar 

  25. Falkowski PG, Fenchel T, Delong EF (2008) The microbial engines that drive Earth’s biogeochemical cycles. Science 320(5879):1034–1039. https://doi.org/10.1126/science.1153213

    CAS  Article  PubMed  Google Scholar 

  26. Hartmann M, Frey B, Mayer J, Mäder P, Widmer F (2015) Distinct soil microbial diversity under long-term organic and conventional farming. ISME J 9(5):1177. https://doi.org/10.1038/ismej.2014.210c

    Article  PubMed  Google Scholar 

  27. Li HW, Zhi XY, Yao JC, Zhou Y, Tang SK, Klenk HP, Zhao J, Li WJ (2013) Comparative genomic analysis of the genus Nocardiopsis provides new insights into its genetic mechanisms of environmental adaptability. PLoS One. https://doi.org/10.1371/journal.pone.0061528

    Article  PubMed  PubMed Central  Google Scholar 

  28. Rodriguez-R LM, Gunturu S, Harvey WT, Rosselló-Mora R, Tiedje JM, Cole JR, Konstantinidis KT (2018) The Microbial Genomes Atlas (MiGA) webserver: taxonomic and gene diversity analysis of Archaea and Bacteria at the whole genome level. Nucleic Acids Res. https://doi.org/10.1093/nar/gky467

    Article  PubMed  PubMed Central  Google Scholar 

  29. Bennur T, Kumar AR, Zinjarde S, Javdekar V (2015) Nocardiopsis species: incidence, ecological roles and adaptations. Microbiol Res 174:33–47. https://doi.org/10.1016/j.micres.2015.03.010

    Article  PubMed  Google Scholar 

  30. Legendre P, L Legendre (1998) Numerical ecology, 2nd English edn. Elsevier, p 853

  31. Langenheder S, Bulling MT, Solan M, Prosser JI (2010) Bacterial biodiversity-ecosystem functioning relations are modified by environmental complexity. PLoS One 5(5):10834. https://doi.org/10.1371/journal.pone.0010834

    CAS  Article  Google Scholar 

  32. Sjöstedt J, Langenheder S, Kritzberg E, Karlsson CM, Lindström ES (2018) Repeated disturbances affect functional but not compositional resistance and resilience in an aquatic bacterioplankton community. Environ Microbiol Rep 10(4):493–500. https://doi.org/10.1111/1758-2229.12656

    CAS  Article  PubMed  Google Scholar 

  33. Margesin R, Zimmerbauer A, Schinner F (1999) Soil lipase activity–a useful indicator of oil biodegradation. Biotechnol Tech 13(12):859–863. https://doi.org/10.1023/A:1008928308695

    CAS  Article  Google Scholar 

  34. Ramos PL, Kondo MY, Santos SM, de Vasconcellos SP, Rocha RC, da Cruz JB, Eugenio PF, Cabral H, Juliano MA, Juliano L, Setubal JC (2018) A tropical composting operation unit at são paulo zoo as a source of bacterial proteolytic enzymes. Appl Biochem Biotechnol. https://doi.org/10.1007/s12010-018-2810-7

    Article  PubMed  Google Scholar 

  35. Kadri T, Rouissi T, Magdouli S, Brar SK, Hegde K, Khiari Z, Daghrir R, Lauzon JM (2018) Production and characterization of novel hydrocarbon degrading enzymes from Alcanivorax borkumensis. Int J Biol Macromol 112:230–240. https://doi.org/10.1016/j.ijbiomac.2018.01.177

    CAS  Article  PubMed  Google Scholar 

  36. Sharma AK, Kikani BA, Singh SP (2020) Biochemical, thermodynamic and structural characteristics of a biotechnologically compatible alkaline protease from a haloalkaliphilic, Nocardiopsis dassonvillei OK-18. Int J Biol Macromol 153:680–696. https://doi.org/10.1016/j.ijbiomac.2020.03.006

    CAS  Article  PubMed  Google Scholar 

  37. Gohel SD, Singh SP (2017) Morphological, cultural and molecular diversity of the salt-tolerant alkaliphilic actinomycetes from saline habitats. In: Bhukya B, Tangutur AD (eds) Microbial biotechnology: technological challenges and developmental trends. CRC Press, Boca Raton, p 337

    Chapter  Google Scholar 

  38. Gunde-Cimerman N, Plemenitas A, Oren A (2018) Strategies of adaptation of microorganisms of the three domains of life to high salt concentrations. FEMS Microbiol Rev 42(3):353–375. https://doi.org/10.1093/femsre/fuy009

    CAS  Article  PubMed  Google Scholar 

  39. Jiang S, Sun W, Chen M, Dai S, Zhang L, Liu Y (2007) Diversity of culturable actinobacteria isolated from marine sponge Haliclona sp.. Anton Leeuw Int J G 92:405–416. https://doi.org/10.1007/s10482-007-9169-z

    CAS  Article  Google Scholar 

  40. Binayke A, Ghorbel S, Hmidet N, Raut A, Gunjal A, Uzgare A, Patil N, Waghmode M, Nawani N (2018) Analysis of diversity of actinomycetes from arid and saline soils at Rajasthan, India. Environ Sustain. https://doi.org/10.1007/s42398-018-0003-5

    Article  Google Scholar 

  41. Litzner BR, Caton TM, Schneegurt MA (2006) Carbon substrate utilization, antibiotic sensitivity, and numerical taxonomy of bacterial isolates from the Great Salt Plains of Oklahoma. Arch Microbiol 185(4):286–296. https://doi.org/10.1007/s00203-006-0096-6

    CAS  Article  PubMed  Google Scholar 

  42. Zeng YX, Yu Y, Qiao ZY, Jin HY, Li HR (2014) Diversity of bacterioplankton in coastal seawaters of Fildes Peninsula, King George Island. Antarctica Arch Microbiol 196(2):137–147. https://doi.org/10.1007/s00203-013-0950-2

    CAS  Article  PubMed  Google Scholar 

  43. Mahbub KR, Subashchandrabose SR, Krishnan K, Naidu R, Megharaj M (2017) Mercury alters the bacterial community structure and diversity in soil even at concentrations lower than the guideline values. Appl Microbiol Biotechnol 101(5):2163–2175. https://doi.org/10.1007/s00253-016-7965-y

    CAS  Article  PubMed  Google Scholar 

  44. Lutz S, Anesio AM, Edwards A, Benning LG (2017) Linking microbial diversity and functionality of arctic glacial surface habitats. Environ Microbiol 19(2):551–565. https://doi.org/10.1111/1462-2920.13494

    CAS  Article  PubMed  Google Scholar 

  45. Zilber-Rosenberg I, Rosenberg E (2008) Role of microorganisms in the evolution of animals and plants: the hologenome theory of evolution. FEMS Microbiol Rev 32(5):723–735. https://doi.org/10.1111/j.1574-6976.2008.00123.x

    CAS  Article  PubMed  Google Scholar 

  46. Stackebrandt E (1988) Phylogenetic relationships vs. phenotypic diversity: how to achieve a phylogenetic classification system of the eubacteria. Can J Microbiol 34(4):552–556. https://doi.org/10.1139/m88-094

    CAS  Article  PubMed  Google Scholar 

  47. Petraitis PS, Latham RE, Niesenbaum RA (1989) The maintenance of species diversity by disturbance. Q Rev Biol 64(4):393–418

    Article  Google Scholar 

  48. Boon AR, Duineveld GCA, Berghuis EM, Van der Weele JA (1998) Relationships between benthic activity and the annual phytopigment cycle in near-bottom water and sediments in the southern North Sea. Estuarine Coastal Shelf Sci 46(1):1–13. https://doi.org/10.1006/ecss.1997.0264

    Article  Google Scholar 

  49. Rudramurthy M, Sumangala B, Honnavar P, Madhav YB, Munegowda KC, Ravi D (2012) Nasal vestibulitis due to Nocardiopsis dassonvillei in a diabetic patient. J Med Microbiol 61:1168–1173. https://doi.org/10.1099/jmm.0.038240-0

    CAS  Article  Google Scholar 

  50. Barberis C, Almuzara M, Join-Lambert O, Ramírez MS, Famiglietti A, Vay C (2014) Comparison of the Bruker MALDI-TOF mass spectrometry system and conventional phenotypic methods for identification of Gram-positive rods. PLoS One. https://doi.org/10.1371/journal.pone.0106303

    Article  PubMed  PubMed Central  Google Scholar 

  51. Embley TM, Stackebrandt E (1994) The molecular phylogeny and systematics of the actinomycetes. Annu Rev Microbiol 48(1):257–289. https://doi.org/10.1146/annurev.mi.48.100194.001353

    CAS  Article  PubMed  Google Scholar 

  52. Thakrar FJ, Singh SP (2019) Catalytic, thermodynamic and structural properties of an immobilized and highly thermostable alkaline protease from a haloalkaliphilic actinobacteria, Nocardiopsis alba Tata-5. Bioresour Technol 278:150–158. https://doi.org/10.1016/j.biortech.2019.01.058

    CAS  Article  PubMed  Google Scholar 

  53. Raiyani NM, Singh SP (2020) Taxonomic and functional profiling of the microbial communities of Arabian Sea: a metagenomics approach. Genomics 112:4361–4369. https://doi.org/10.1016/j.ygeno.2020.07.024

    CAS  Article  PubMed  Google Scholar 

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Acknowledgements

Financial assistance and JRF/SRF to DR and MS under a Net Working Project of the Ministry of Earth Sciences, New Delhi, is duly acknowledged. Sincere thanks are also due to Prof. Bharti Dave, Coordinator, MoES Networking Project for providing the physicochemical data. The authors are thankful to Saurashtra University for financial and infrastructural support. The facilities created under various UGC Programmes, including CAS, DST-FIST and DBT-Multi-institutional Programmes, are also acknowledged. SPS acknowledges DST-SERB International Travel Support to present his research in the ‘Extremophile 2016,’ Kyoto, Japan.

Funding

This study was funded by the Ministry of Earth Sciences (MoES) Government of India, New Delhi (MoES/16/06/2013-RDEAS Dated: 23/10/2015).

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DSR executed the experiment, analyzed the data and wrote the manuscript; MAS assisted in actinomycetes cultivation; SDG assisted in biochemical tests; and SPS planned and designed the experiments and critically examined the data and the manuscript.

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Correspondence to Satya P. Singh.

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Rathore, D.S., Sheikh, M.A., Gohel, S.D. et al. Genetic and Phenotypic Heterogeneity of the Nocardiopsis alba Strains of Seawater. Curr Microbiol 78, 1377–1387 (2021). https://doi.org/10.1007/s00284-021-02420-0

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