Genetic and Phenotypic Heterogeneity of the Nocardiopsis alba Strains of Seawater.
Journal
Current microbiology
ISSN: 1432-0991
Titre abrégé: Curr Microbiol
Pays: United States
ID NLM: 7808448
Informations de publication
Date de publication:
Apr 2021
Apr 2021
Historique:
received:
20
07
2020
accepted:
10
02
2021
pubmed:
2
3
2021
medline:
15
5
2021
entrez:
1
3
2021
Statut:
ppublish
Résumé
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.
Identifiants
pubmed: 33646381
doi: 10.1007/s00284-021-02420-0
pii: 10.1007/s00284-021-02420-0
doi:
Substances chimiques
DNA, Bacterial
0
RNA, Ribosomal, 16S
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
1377-1387Subventions
Organisme : Ministry of Earth Sciences New Delhi
ID : MoES/16/06/2013-RDEAS Dated: 23/10/2015
Références
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
doi: 10.1007/s00248-004-0211-7
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
doi: 10.1007/s00203-018-1484-4
pubmed: 29396619
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
doi: 10.36877/pmmb.a0000009
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
doi: 10.1007/s00248-017-0930-1
pubmed: 28105510
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
doi: 10.1139/W07-060
pubmed: 17898855
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
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
doi: 10.1007/s13205-017-1075-0
pubmed: 29354364
pmcid: 5754276
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)
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
doi: 10.6024/jmbai.2019.61.1.2028-11
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
doi: 10.1080/01490451.2018.1471107
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
APHA–American Public Health Association (2012) Standard methods for the examination of water and wastewater, 22nd edn. American Public Health Association, Washington, DC
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
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
doi: 10.3389/fmicb.2020.00941
pubmed: 32582046
pmcid: 7283590
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
doi: 10.1016/j.micres.2005.08.004
pubmed: 16765838
Greenacre M (2017) Correspondence analysis in practice. Chapman and Hall/CRC.
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
doi: 10.1016/j.apjtb.2015.04.007
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
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
doi: 10.1111/1574-6941.12437
pubmed: 25314312
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
doi: 10.2307/1938672
Tendler MD, Burkholder PR (1961) Studies on the thermophilic actinomycetes: i methods of cultivation. Appl Environ Microbiol 9(5):394–399
doi: 10.1128/AM.9.5.394-399.1961
Ackermann M (2015) A functional perspective on phenotypic heterogeneity in microorganisms. Nat Rev Microbiol 13(8):497–508. https://doi.org/10.1038/nrmicro3491
doi: 10.1038/nrmicro3491
pubmed: 26145732
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
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
doi: 10.1016/j.wasman.2009.12.008Get
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
doi: 10.1126/science.1153213
pubmed: 18497287
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
doi: 10.1038/ismej.2014.210c
pubmed: 25350160
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
doi: 10.1371/journal.pone.0061528
pubmed: 24400037
pmcid: 3877406
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
doi: 10.1093/nar/gky467
pubmed: 29905870
pmcid: 6031002
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
doi: 10.1016/j.micres.2015.03.010
pubmed: 25946327
Legendre P, L Legendre (1998) Numerical ecology, 2nd English edn. Elsevier, p 853
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
doi: 10.1371/journal.pone.0010834
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
doi: 10.1111/1758-2229.12656
pubmed: 29733107
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
doi: 10.1023/A:1008928308695
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
doi: 10.1007/s12010-018-2810-7
pubmed: 29936594
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
doi: 10.1016/j.ijbiomac.2018.01.177
pubmed: 29386098
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
doi: 10.1016/j.ijbiomac.2020.03.006
pubmed: 32145232
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
doi: 10.1201/b19978-22
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
doi: 10.1093/femsre/fuy009
pubmed: 29529204
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
doi: 10.1007/s10482-007-9169-z
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
doi: 10.1007/s42398-018-0003-5
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
doi: 10.1007/s00203-006-0096-6
pubmed: 16518618
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
doi: 10.1007/s00203-013-0950-2
pubmed: 24408126
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
doi: 10.1007/s00253-016-7965-y
pubmed: 27873000
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
doi: 10.1111/1462-2920.13494
pubmed: 27511455
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
doi: 10.1111/j.1574-6976.2008.00123.x
pubmed: 18549407
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
doi: 10.1139/m88-094
pubmed: 3052761
Petraitis PS, Latham RE, Niesenbaum RA (1989) The maintenance of species diversity by disturbance. Q Rev Biol 64(4):393–418
doi: 10.1086/416457
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
doi: 10.1006/ecss.1997.0264
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
doi: 10.1099/jmm.0.038240-0
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
doi: 10.1371/journal.pone.0106303
pubmed: 25184254
pmcid: 4153636
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
doi: 10.1146/annurev.mi.48.100194.001353
pubmed: 7529976
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
doi: 10.1016/j.biortech.2019.01.058
pubmed: 30685619
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
doi: 10.1016/j.ygeno.2020.07.024
pubmed: 32712295