Deciphering Toxic Pollutants Breakdown Potential in Microbial Community of Chumathang Hot Spring, Ladakh, India via Shotgun Metagenome Sequencing.


Journal

Current microbiology
ISSN: 1432-0991
Titre abrégé: Curr Microbiol
Pays: United States
ID NLM: 7808448

Informations de publication

Date de publication:
29 Oct 2024
Historique:
received: 12 04 2024
accepted: 18 09 2024
medline: 29 10 2024
pubmed: 29 10 2024
entrez: 29 10 2024
Statut: epublish

Résumé

Persistent Organic Pollutants (POPs) have been in focus of research due to their massive contamination of environment and bio-accumulation. Bioremediation and high-throughput research have gained momentum to curb the harmful effects of POPs. The present research has explored the microbial diversity of Chumathang Hot Spring, Ladakh, India, through Illumina metagenomic HiSeq 4000 sequencing platform and their potential to degrade persistent pollutants, especially xenobiotics. Taxonomic characterization based on raw metagenomic data illuminated the abundance of members of Pseudomonadota and Actinomyceota. The re-construction of the microbial genomes from assembled contigs and scaffolds using de novo assembler metaSPAdes and their further annotation through contig alignment with available reference genomes elucidated the landscape of the hot spring's microbes. The predominantly occupied key genera reported were Pannonibacter and Novosphingobium. Comparative genomic analysis established evolutionary relationships and functional diversities among hot spring microbial communities. The function annotation through MG-RAST has revealed their metabolic versatility of degrading a wide array of xenobiotic compounds, including caprolactam, dioxin, chlorobenzene, benzoate, and. Further, the hydroxylating dioxygenase (Saro_3901) was identified as a pivotal component in the aromatic degradation pathways, showcasing extensive metabolic interconnectivity. Interestingly, protein interaction network analysis identified hub genes like Saro_1233 (protocatechuate 4,5-dioxygenase alpha subunit), while Saro_3057 (amidase) was noted for its critical role in network communication and control. The resilience of thermal ecosystems, evidenced by robust enzymatic activity and degradation capability among organisms with < 95% genetic similarity, underscores their potential for industrial and bioremediation exploration, emphasizing the importance of preserving and studying biodiverse habitats.

Identifiants

pubmed: 39467883
doi: 10.1007/s00284-024-03915-2
pii: 10.1007/s00284-024-03915-2
doi:

Substances chimiques

Persistent Organic Pollutants 0
Xenobiotics 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

430

Informations de copyright

© 2024. The Author(s), under exclusive licence to Springer Science+Business Media, LLC, part of Springer Nature.

Références

Saini N, Pal K, Sujata BD, Sharma M (2021) Thermophilic algae: a new prospect towards environmental sustainability. J Clean Prod 324:129277. https://doi.org/10.1016/j.jclepro.2021.129277
doi: 10.1016/j.jclepro.2021.129277
Mishra S, Lin Z, Pang S, Zhang W, Bhatt P, Chen S (2021) Recent advanced technologies for the characterization of xenobiotic-degrading microorganisms and microbial communities. Front Bioeng Biotechnol 9:31. https://doi.org/10.3389/fbioe.2021.632059
doi: 10.3389/fbioe.2021.632059
Tyler CR, Jobling S, Sumpter JP (1998) Endocrine disruption in wildlife: a critical review of the evidence. Crit Rev Toxicol 28:319–361. https://doi.org/10.1080/10408449891344236
doi: 10.1080/10408449891344236 pubmed: 9711432
Liu L, Bilal M, Duan X, Iqbal HMN (2019) Mitigation of environmental pollution by genetically engineered bacteria—current challenges and future perspectives. Sci Tot Env 667:444–454. https://doi.org/10.1016/j.scitotenv.2019.02.390
doi: 10.1016/j.scitotenv.2019.02.390
Desai AM, Autenrieth RL, Dimitriou-Christidis P, McDonald TJ (2008) Biodegradation kinetics of select polycyclic aromatic hydrocarbon (PAH) mixtures by Sphingomonas paucimobilis EPA505. Biodegradation 19:223–233. https://doi.org/10.1007/s10532-007-9129-3
doi: 10.1007/s10532-007-9129-3 pubmed: 17534722
D’Argenio V, Notomista E, Petrillo M, Cantiello P, Cafaro V, Izzo V et al (2014) Complete sequencing of Novosphingobium sp. PP1Y reveals a biotechnologically meaningful metabolic pattern. BMC Genomics 15:1–14. https://doi.org/10.1186/1471-2164-15-384
doi: 10.1186/1471-2164-15-384
Fredrickson JK, Brockman FJ, Workman DJ, Li SW, Stevens TO (1991) Isolation and characterization of a subsurface bacterium capable of growth on toluene, naphthalene, and other aromatic compounds. Appl Environ Microbiol 57:796–803. https://doi.org/10.1128/aem.57.3.796-803.1991
doi: 10.1128/aem.57.3.796-803.1991 pubmed: 16348445 pmcid: 182797
Toyama T, Kainuma Y, Kikuchi S, Mori K (2012) Biodegradation of bisphenol A and 4-alkylphenols by Novosphingobium sp. strain TYA-1 and its potential for treatment of polluted water. Water Sci Technol 66:2202–2208. https://doi.org/10.2166/wst.2012.453
doi: 10.2166/wst.2012.453 pubmed: 22949252
Mehetre G, Shah M, Dastager SG, Dharne MS (2018) Untapped bacterial diversity and metabolic potential within unkeshwar hot springs, India. Arch Microbiol 200:753–770. https://doi.org/10.1007/s00203-018-1484-4
doi: 10.1007/s00203-018-1484-4 pubmed: 29396619
Saini N, Aamir M, Singh VK, Deepak B, Mona S (2023) Unveiling the microbial diversity and functional dynamics of Shiv Kund, Sohna hot spring, India through a shotgun metagenomics approach. Arch Microbiol 205:323. https://doi.org/10.1007/s00203-023-03664-z
doi: 10.1007/s00203-023-03664-z pubmed: 37651004
Malesevic M, Stanisavljevic N, Matijasevic D, Curcic J, Tasic V, Tasic S et al (2023) Metagenomic analysis of bacterial community and isolation of representative strains from vranjska banja hot spring, Serbia. Microb Ecol 1:1–13. https://doi.org/10.1007/s00248-023-02242-6
doi: 10.1007/s00248-023-02242-6
Caspers H (1979) F. J. H. Mackereth, J. Heron & J. F. Talling (1979) Water analysis: Some revised methods for limnologists. Far Sawrey Ambleside: Freshwater Biological Association Scientific Publication. Intl Review of Hydrobiology, https://doi.org/10.1002/iroh.19790640404 .
Smith DJ, Berry MA, Cory RM, Johengen TH, Kling GW, Davis TW et al (2022) Heterotrophic bacteria dominate catalase expression during microcystis blooms. Appl Environ Microbiol 88:e02544-e2621. https://doi.org/10.1128/aem.02544-21
doi: 10.1128/aem.02544-21 pubmed: 35862723 pmcid: 9328184
Abdel-Latif A, Osman G (2017) Comparison of three genomic DNA extraction methods to obtain high DNA quality from maize. Plant Methods 13:1–9. https://doi.org/10.1186/s13007-016-0152-4
doi: 10.1186/s13007-016-0152-4 pubmed: 28053646 pmcid: 5209869
Castañeda-Rico S, León-Paniagua L, Edwards CW, Maldonado JE (2020) Ancient DNA from museum specimens and next generation sequencing help resolve the controversial evolutionary history of the critically endangered puebla deer mouse. Front Ecol Evol 8:94. https://doi.org/10.3389/fevo.2020.00094
doi: 10.3389/fevo.2020.00094
Nagar S, Talwar C, Motelica-Heino M, Richnow HH, Shakarad M, Lal R et al (2022) Microbial ecology of sulfur biogeochemical cycling at a mesothermal hot spring atop Northern Himalayas. India Front Microbiol 13:848010. https://doi.org/10.3389/fmicb.2022.848010
doi: 10.3389/fmicb.2022.848010 pubmed: 35495730
Chen S, Huang T, Zhou Y, Han Y, Xu M, Gu J et al (2017) AfterQC: automatic filtering, trimming, error removing and quality control for fastq data. BMC Bioinf 18:91. https://doi.org/10.1186/s12859-017-1469-3
doi: 10.1186/s12859-017-1469-3
Vosloo S, Huo L, Anderson CL, Dai Z, Sevillano M, Pinto A et al (2021) Evaluating de novo assembly and binning strategies for time series drinking water metagenomes. Microbiol Spectr 9:e01434-e1521. https://doi.org/10.1128/Spectrum.01434-21
doi: 10.1128/Spectrum.01434-21 pubmed: 34730411 pmcid: 8567270
Eren AM, Vineis JH, Morrison HG, Sogin ML (2013) A filtering method to generate high quality short reads using illumina paired-end technology. PLoS ONE 8:e66643. https://doi.org/10.1371/annotation/afa5c40d-c604-46ae-84c4-82cb92193a5e
doi: 10.1371/annotation/afa5c40d-c604-46ae-84c4-82cb92193a5e pubmed: 23799126 pmcid: 3684618
Wood DE, Lu J, Langmead B (2019) Improved metagenomic analysis with Kraken 2. Genome Biol 20:1–13. https://doi.org/10.1186/s13059-019-1891-0
doi: 10.1186/s13059-019-1891-0
SILVAngs. https://ngs.arb-silva.de/silvangs/ . Accessed 22 Nov 2023
Apostolopoulos N, Glaeser SP, Bagwe R, Janssen S, Mayer U, Ewers C et al (2021) Description and comparison of the skin and ear canal microbiota of non-allergic and allergic German shepherd dogs using next generation sequencing. PLoS ONE 16:e0250695. https://doi.org/10.1371/journal.pone.0250695
doi: 10.1371/journal.pone.0250695 pubmed: 33939741 pmcid: 8092680
Nurk S, Meleshko D, Korobeynikov A, Pevzner PA (2017) metaSPAdes: a new versatile metagenomic assembler. Genome Res 27:824–834. https://doi.org/10.1101/gr.213959.116
doi: 10.1101/gr.213959.116 pubmed: 28298430 pmcid: 5411777
Prjibelski A, Antipov D, Meleshko D, Lapidus A, Korobeynikov A (2020) Using SPAdes De Novo assembler. Curr Protoc Bioinformatics 70:e102. https://doi.org/10.1002/cpbi.102
doi: 10.1002/cpbi.102 pubmed: 32559359
Liu L, Wang Y, Che Y, Chen Y, Xia Y, Luo R et al (2020) High-quality bacterial genomes of a partial-nitritation/anammox system by an iterative hybrid assembly method. Microbiome 8:1–17. https://doi.org/10.1186/s40168-020-00937-3
doi: 10.1186/s40168-020-00937-3
Deforche K (2017) An alignment method for nucleic acid sequences against annotated genomes. bioRxiv. https://doi.org/10.1101/200394
doi: 10.1101/200394
Arahal DR (2014) Whole-genome analyses: average nucleotide identity. In: Goodfellow M, Sutcliffe I, Chun J (eds) Methods in microbiology. Elsevier, Hoboken, pp 103–122. https://doi.org/10.1016/bs.mim.2014.07.002
doi: 10.1016/bs.mim.2014.07.002
Grant JR, Enns E, Marinier E, Mandal A, Herman EK, Chen CY et al (2023) Proksee: in-depth characterization and visualization of bacterial genomes. Nucleic Acids Res 51:W484–W492. https://doi.org/10.1093/nar/gkad326
doi: 10.1093/nar/gkad326 pubmed: 37140037 pmcid: 10320063
Home-Genome-NCBI. https://www.ncbi.nlm.nih.gov/genome/ . Accessed 20 Mar 2024
Bacterial and Viral Bioinformatics Resource Center | BV-BRC. https://www.bv-brc.org/ . Accessed 20 Mar 2024
Keegan KP, Glass EM, Meyer F (2016) MG-RAST, a metagenomics service for analysis of microbial community structure and function. In: Martin F, Uroz S (eds) Methods in molecular biology. Humana Press, New York, pp 207–233. https://doi.org/10.1007/978-1-4939-3369-3_13
doi: 10.1007/978-1-4939-3369-3_13
BioCyc Pathway/Genome Database Collection. https://biocyc.org/ . Accessed 20 Mar 2024
STRING: functional protein association networks. https://string-db.org/ . Accessed 22 Nov 2023
Szklarczyk D, Franceschini A, Wyder S, Forslund K, Heller D, Huerta-Cepas J et al (2015) STRING v10: protein–protein interaction networks, integrated over the tree of life. Nucleic Acids Res 43:D447–D452. https://doi.org/10.1093/nar/gku1003
doi: 10.1093/nar/gku1003 pubmed: 25352553
Shannon P, Markiel A, Ozier O, Forslund K, Heller D, Huerta-Cepas J et al (2003) Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res 13:2498–2504. https://doi.org/10.1101/gr.1239303
doi: 10.1101/gr.1239303 pubmed: 14597658 pmcid: 403769
Biswas A, Sharma SP (2020) Advances in modeling and interpretation in near surface geophysics. Springer Cham. https://doi.org/10.1007/978-3-030-28909-6
doi: 10.1007/978-3-030-28909-6
Craig J, Absar A, Bhat G, Cadel G, Hafiz M, Hakhoo N et al (2013) Hot springs and the geothermal energy potential of Jammu & Kashmir State, N.W. Himalaya. India Earth Sci Rev 126:156–177. https://doi.org/10.1016/j.earscirev.2013.05.004
doi: 10.1016/j.earscirev.2013.05.004
Rawat G, Bartarya SK, Singh B, Bhasin RK (2020) Geophysical characterization of chumathang (Ladakh) hot spring. In: Biswas A, Sharma S (eds) Advances in modeling and interpretation in near surface geophysics Springer geophysics. Springer, Cham, pp 363–376
doi: 10.1007/978-3-030-28909-6_13
Mir AR, Dar FA, Ahmad MZ (2023) Characteristics of geosites for promotion and development of geotourism in Ladakh, India. Geoheritage 15:1–16. https://doi.org/10.1007/s12371-023-00866-1
doi: 10.1007/s12371-023-00866-1
Debnath T, Deb S, Das SK (2023) Influence of geochemistry in the tropical hot springs on microbial community structure and function. Curr Microbiol 80:1–12. https://doi.org/10.1007/s00284-022-03118-7
doi: 10.1007/s00284-022-03118-7
Wu L, Long H, Huang S, Niu X, Li S, Yu X et al (2023) Bacterial diversity in water from Xifeng hot spring in China. Braz J Microbiol 54:1943–1954. https://doi.org/10.1007/s42770-023-01070-7
doi: 10.1007/s42770-023-01070-7 pubmed: 37594656 pmcid: 10484846
Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P et al (2013) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 41:D590–D596. https://doi.org/10.1093/nar/gks1219
doi: 10.1093/nar/gks1219 pubmed: 23193283
Bandyopadhyay S, Schumann P, Das SK (2013) Pannonibacter indica sp. nov., a highly arsenate-tolerant bacterium isolated from a hot spring in India. Arch Microbiol 195:1–8. https://doi.org/10.1007/s00203-012-0840-z
doi: 10.1007/s00203-012-0840-z pubmed: 22940883
Xian WD, Li MM, Salam N, Ding YP, Zhou EM, Yin YR et al (2019) Novosphingobium meiothermophilum sp. Nov., isolated from a hot spring. Int J Syst Evol Microbiol 69:1737–1743. https://doi.org/10.1099/ijsem.0.003384
doi: 10.1099/ijsem.0.003384 pubmed: 30958256
Saini N, Kumar S, Deepak B, Mona S (2022) High-throughput sequencing technologies in metagenomics. In: Kumar V, Thakur IS (eds) Omics insights in environmental bioremediation. Springer, Singapore, pp 545–569. https://doi.org/10.1007/978-981-19-4320-1_23
doi: 10.1007/978-981-19-4320-1_23
Stolz A (2009) Molecular characteristics of xenobiotic-degrading sphingomonads. Appl Microbiol Biotechnol 81:793–811. https://doi.org/10.1007/s00253-008-1752-3
doi: 10.1007/s00253-008-1752-3 pubmed: 19002456
Najar IN, Sherpa MT, Das S, Thakur N (2020) Bacterial diversity and functional metagenomics expounding the diversity of xenobiotics, stress, defense and CRISPR gene ontology providing eco-efficiency to Himalayan hot springs. Funct Integr Genomics 20:479–496. https://doi.org/10.1007/s10142-019-00723-x
doi: 10.1007/s10142-019-00723-x pubmed: 31897823
Kumagawa E, Katsumata M, Nishimura H, Watanabe T, Ishii SI, Ohta Y (2023) The etherase system of Novosphingobium sp. MBES04 functions as a sensor of lignin fragments through phenylpropanone production to induce specific transcriptional responses. Environ Microbiol Rep 16:e13210. https://doi.org/10.1111/1758-2229.13210
doi: 10.1111/1758-2229.13210 pubmed: 37950419 pmcid: 10866074
Kumar R, Verma H, Haider S, Bajaj A, Sood U, Ponnusamy K et al (2017) Comparative genomic analysis reveals habitat-specific genes and regulatory hubs within the genus novosphingobium. mSystems 2:10–1128. https://doi.org/10.1128/msystems.00020-17
doi: 10.1128/msystems.00020-17
Noguera et al. 2021, United States Patent US 11,981,946 B2. warf.org. https://www.warf.org/wp-content/uploads/technologies/ipstatus/P180219US03.pdf .

Auteurs

Neha Saini (N)

Department of Environmental Science & Engineering, Guru Jambheshwar University of Science & Technology, Hisar, Haryana, 125001, India.

Mohd Aamir (M)

Division of Plant Pathology, ICAR- Indian Agricultural Research Institute, Pusa, New Delhi, 110012, India.
Department of Life Sciences, Parul Institute of Applied Sciences, Parul University, Vadodara, Gujarat, 391760, India.

Zainul Abdeen Khan (ZA)

Division of Plant Pathology, Advanced Centre for Plant Virology, ICAR-Indian Agricultural Research Institute, New Delhi, 110012, India.

Vinay Kumar Singh (VK)

Centre for Bioinformatics, School of Biotechnology, Banaras Hindu University, Varanasi, 221005, India.

Pankaj Sah (P)

Applied Sciences Department, College of Applied Sciences and Pharmacy, University of Technology and Applied Sciences, Al Khuwair, PO Box 74, Muscat, 133, Sultanate of Oman.

Sharma Mona (S)

Department of Environmental Studies, School of Interdisciplinary and Applied Sciences, Central University of Haryana, Mahendergarh, Haryana, 123031, India. mona@cuh.ac.in.

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