Skip to main content

Advertisement

SpringerLink
Log in

Genome-scale revealing the central metabolic network of the fast growing methanotroph Methylomonas sp. ZR1

  • Original Paper
  • Published:
World Journal of Microbiology and Biotechnology Aims and scope Submit manuscript

Abstract

Methylomonas sp. ZR1 was an isolated new methanotrophs that could utilize methane and methanol growing fast and synthesizing value added compounds such as lycopene. In this study, the genomic study integrated with the comparative transcriptome analysis were taken to understanding the metabolic characteristic of ZR1 grown on methane and methanol at normal and high temperature regime. Complete Embden-Meyerhof-Parnas pathway (EMP), Entner–Doudoroff pathway (ED), Pentose Phosphate Pathway (PP) and Tricarboxy Acid Cycle (TCA) were found to be operated in ZR1. In addition, the energy saving ppi-dependent EMP enzyme, coupled with the complete and efficient central carbon metabolic network might be responsible for its fast growing nature. Transcript level analysis of the central carbon metabolism indicated that formaldehyde metabolism was a key nod that may be in charge of the carbon conversion efficiency (CCE) divergent of ZR1 grown on methanol and methane. Flexible nitrogen and carotene metabolism pattern were also investigated in ZR1. Nitrogenase genes in ZR1 were found to be highly expressed with methane even in the presence of sufficient nitrate. It appears that, higher lycopene production in ZR1 grown on methane might be attributed to the higher proportion of transcript level of C40 to C30 metabolic gene. Higher transcript level of exopolysaccharides metabolic gene and stress responding proteins indicated that ZR1 was confronted with severer growth stress with methanol than with methane. Additionally, lower transcript level of the TCA cycle, the dramatic high expression level of the nitric oxide reductase and stress responding protein, revealed the imbalance of the central carbon and nitrogen metabolic status, which would result in the worse growth of ZR1 with methanol at 30 °C.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Abhay Ku AS, Pakrasi H, Kishore GM (2016) Amino acid producing microorganisms and methods of making and using. United State Patent Application 20160369311

  • Akberdin IR, Thompson M, Hamilton R et al (2018) Methane utilization in Methylomicrobium alcaliphilum 20Z(R): a systems approach. Sci Rep 8(1):2512

    Article  PubMed  PubMed Central  Google Scholar 

  • Anders S, Huber W (2010) Differential expression analysis for sequence count data. Genome Biol 11(10):R106

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Anders S, Pyl PT, Huber W (2015) HTSeq – a Python framework to work with high-throughput sequencing data. Bioinformatics 31(2):166–169

    Article  CAS  PubMed  Google Scholar 

  • Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M, Kulikov AS, Lesin VM, Nikolenko SI, Pham S, Prjibelski AD, Pyshkin AV, Sirotkin AV, Vyahhi N, Tesler G, Alekseyev MA, Pevzner PA (2012) SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 19(5):455–477

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Benson DA, Karsch-Mizrachi I, Clark K, Lipman DJ, Ostell J, Sayers EW (2012) GenBank. Nucleic Acids Res 40(Database issue):D48–D53

    Article  CAS  PubMed  Google Scholar 

  • Cantera S, Munoz R, Lebrero R et al (2018) Technologies for the bioconversion of methane into more valuable products. Curr Opin Biotechnol 50:128–135

    Article  CAS  PubMed  Google Scholar 

  • Cheng Q (2006) Structural diversity and functional novelty of new carotenoid biosynthesis genes. J Ind Microbiol Biotechnol 33(7):552–559

    Article  CAS  PubMed  Google Scholar 

  • Clomburg JM, Crumbley AM, Gonzalez R (2017) Industrial biomanufacturing: the future of chemical production. Science 355

  • de la Torre A, Metivier A, Chu F, Laurens LM, Beck DA, Pienkos PT, Lidstrom ME, Kalyuzhnaya MG (2015) Genome-scale metabolic reconstructions and theoretical investigation of methane conversion in Methylomicrobium buryatense strain 5G(B1). Microb Cell Factories 14:188

    Article  Google Scholar 

  • Delcher AL, Bratke KA, Powers EC, Salzberg SL (2007) Identifying bacterial genes and endosymbiont DNA with glimmer. Bioinformatics 23(6):673–679

    Article  CAS  PubMed  Google Scholar 

  • Dispirito AA, kunz RC, Choi D-W et al (2004) Respiration in methanotrophs. In: Zannoni D (ed) Diversity of prokaryotic respiratory system. Springer, p 149

  • Dubois M, Gilles KA, Hamilton JK (1956) Colorimetric method for determination of sugars and related substances. Anal Chem 28(3):7

    Article  Google Scholar 

  • Fu Y, Li Y, Lidstrom M (2017) The oxidative TCA cycle operates during methanotrophic growth of the Type I methanotroph Methylomicrobium buryatense 5GB1. Metab Eng 42:43–51

    Article  CAS  PubMed  Google Scholar 

  • Fu Y, He L, Reeve J et al (2019) Core metabolism shifts during growth on methanol versus methane in the methanotroph Methylomicrobium buryatense 5GB1. mBio 10

  • Gardner SN, Slezak T, Hall BG (2015) kSNP3.0: SNP detection and phylogenetic analysis of genomes without genome alignment or reference genome. Bioinformatics 31(17):2877–2878

    Article  CAS  PubMed  Google Scholar 

  • Gilman A, Laurens LM, Puri AW et al (2015) Bioreactor performance parameters for an industrially-promising methanotroph Methylomicrobium buryatense 5GB1. Microb Cell Factories 14:182

    Article  Google Scholar 

  • Glaeser J, Klug G (2005) Photo-oxidative stress in Rhodobacter sphaeroides: protective role of carotenoids and expression of selected genes. Microbiology 151(Pt 6):1927–1938

    Article  CAS  PubMed  Google Scholar 

  • Guo W, Li D, He R, Wu M, Chen W, Gao F, Zhang Z, Yao Y, Yu L, Chen S (2017) Synthesizing value-added products from methane by a new Methylomonas. J Appl Microbiol 123(5):1214–1227

    Article  CAS  PubMed  Google Scholar 

  • Hamer G (2010) Methanotrophy: from the environment to industry and back. Chem Eng J 160:7

    Article  Google Scholar 

  • Henard CA, Smith H, Dowe N, Kalyuzhnaya MG, Pienkos PT, Guarnieri MT (2016) Bioconversion of methane to lactate by an obligate methanotrophic bacterium. Sci Rep 6:21585

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Henard CA, Akberdin IR, Kalyuzhnaya MG et al (2019) Muconic acid production from methane using rationally-engineered methanotrophic biocatalysts. Green Chem 21:6731–6737

    Article  CAS  Google Scholar 

  • Hoefman S, Dvd H, Boon N, Vandamme P, Vos PD, Heylen K (2014) Niche differentiation in nitrogen metabolism among methanotrophs with an operational taxonomic unit. BMC Microbiol 14:11

    Article  Google Scholar 

  • Hou S, Makarova KS, Saw JH, Senin P, Ly BV, Zhou Z, Ren Y, Wang J, Galperin MY, Omelchenko MV, Wolf YI, Yutin N, Koonin EV, Stott MB, Mountain BW, Crowe MA, Smirnova AV, Dunfield PF, Feng L, Wang L, Alam M (2008) Complete genome sequence of the extremely acidophilic methanotroph isolate V4, Methylacidiphilum infernorum, a representative of the bacterial phylum Verrucomicrobia. Biol Direct 3:26

    Article  PubMed  PubMed Central  Google Scholar 

  • Hur DH, Na J-G, Lee EY (2017) Highly efficient bioconversion of methane to methanol using a novel type I Methylomonas sp. DH-1 newly isolated from brewery waste sludge. J Chem Technol Biotechnol 92(2):311–318

    Article  CAS  Google Scholar 

  • Ivanova EG, Fedorov DN, Doronina NV et al (2006) Production of vitamin B12 in aerobic methylotrophic bacteria. Microbiology 75:494–496

    Article  CAS  Google Scholar 

  • Joergensen L, Degn H (1987) Growth rate and methane affinity of a turbidostatic and oxystatic continuous culture of methylococcus capsulatus bath. Biotechnol Lett 9(1):71–76

    Article  CAS  Google Scholar 

  • Kalyuzhnaya MG, Yang S, Rozova ON, Smalley NE, Clubb J, Lamb A, Gowda GA, Raftery D, Fu Y, Bringel F, Vuilleumier S, Beck DA, Trotsenko YA, Khmelenina VN, Lidstrom ME (2013) Highly efficient methane biocatalysis revealed in a methanotrophic bacterium. Nat Commun 4:2785

    Article  CAS  PubMed  Google Scholar 

  • Kalyuzhnaya MG, Lamb AE, McTaggart TL et al (2015a) Draft genome sequences of gammaproteobacterial methanotrophs isolated from Lake Washington sediment. Genome Announc 3(2)

  • Kalyuzhnaya MG, Puri AW, Lidstrom ME (2015b) Metabolic engineering in methanotrophic bacteria. Metab Eng 29:142–152

    Article  CAS  PubMed  Google Scholar 

  • Kanehisa M, Goto S, Sato Y, Kawashima M, Furumichi M, Tanabe M (2014) Data, information, knowledge and principle: back to metabolism in KEGG. Nucleic Acids Res 42(Database issue):D199–D205

    Article  CAS  PubMed  Google Scholar 

  • Khosravi-Darani K, Mokhtari Z-B, Amai T, Tanaka K (2013) Microbial production of poly(hydroxybutyrate) from C1 carbon sources. Appl Microbiol Biot 97:18

    Google Scholar 

  • 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(Pt 2):346–351

    Article  CAS  PubMed  Google Scholar 

  • Kits KD, Klotz MG, Stein LY (2015) Methane oxidation coupled to nitrate reduction under hypoxia by the Gammaproteobacterium Methylomonas denitrificans, sp. nov. type strain FJG1. Environ Microbiol 17(9):3219–3232

    Article  CAS  PubMed  Google Scholar 

  • Koffas MW, James MD, Schenzle A (2003) High growth methanotrophic bacterial strain Methylomonas 16a. United State Patent 6689601.

  • Konstantinidis KT, Tiedje JM (2005) Genomic insights that advance the species definition for prokaryotes. Proc Natl Acad Sci USA 102(7):2567–2572

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Krieg Wa, emend. Bowman, Sly, et al (2015) Methylomonas. Bergey’s manual of systematics of Archaea and Bacteria, Online John Wiley & Sons, Inc., in association with Bergey’s Manual Trust

  • Leak DJ, Dalton H (1986) Growth yields of methanotrophs 1.Effect of copper on the energetics of methane oxidation. Appl Microbiol Biot (23):7

  • Lee OK, Hur DH, Nguyen DTN, Lee EY (2016) Metabolic engineering of methanotrophs and its application to production of chemicals and biofuels from methane. Biofuels Bioprod Biorefin 10(6):848–863

    Article  CAS  Google Scholar 

  • Lees V, Owens NJP, Murrell JC (1991) Nitrogen metabolism in marine methanotrophs. Arch Microbiol 157:60–65

    Article  CAS  Google Scholar 

  • Lembre P, Lorentz C Di P (2012) Exopolysaccharides of the biofilm matrix: a complex biophysical world

  • Li H, Durbin R (2009) Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25(14):1754–1760

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lidstrom ME (1988) Isolation and characterization of marine methanotrophs. Antonie Van Leeuwenhoek 54:11

    Article  Google Scholar 

  • Liu Y, Lai QL, Goker M, Meier-Kolthoff JP, Wang M, Sun YM, Wang L, Shao ZZ (2015) Genomic insights into the taxonomic status of the Bacillus cereus group. Sci Rep 5

  • Malashenko YR, Pirog TP, Romanovskaya VA et al (2001) Search for methanotrophic producers of exopolysaccharides. Appl Biochem Microbiol 37(6):4

    Article  Google Scholar 

  • Matsen JB, Yang S, Stein LY, Beck D, Kalyuzhnaya MG (2013) Global molecular analyses of methane metabolism in methanotrophic Alphaproteobacterium, Methylosinus trichosporium OB3b. Part I: Transcriptomic study. Front Microbiol 4:40

    Article  PubMed  PubMed Central  Google Scholar 

  • Meier-Kolthoff JP, Auch AF, Klenk HP, Goker M (2013) Genome sequence-based species delimitation with confidence intervals and improved distance functions. BMC Bioinform 14

  • Mohammadi SS, Pol A, van Alen T et al (2017) Ammonia oxidation and nitrite reduction in the verrucomicrobial methanotroph methylacidiphilum fumariolicum SolV. Front Microbiol 8:1901

    Article  PubMed  PubMed Central  Google Scholar 

  • Nguyen A, Hwang I, Lee O et al (2018a) Functional analysis of methylomonas sp. DH-1 genome as a promising biocatalyst for bioconversion of methane to valuable chemicals. Catalysts 8(3):117

    Article  Google Scholar 

  • Nguyen AD, Hwang IY, Lee OK et al (2018b) Systematic metabolic engineering of Methylomicrobium alcaliphilum 20Z for 2,3-butanediol production from methane. Metab Eng 47:323–333

    Article  CAS  PubMed  Google Scholar 

  • Nguyen AD, Kim D, Lee EY (2019a) A comparative transcriptome analysis of the novel obligate methanotroph Methylomonas sp. DH-1 reveals key differences in transcriptional responses in C1 and secondary metabolite pathways during growth on methane and methanol. BMC Genomics 20(1):130

    Article  PubMed  PubMed Central  Google Scholar 

  • Nguyen DTN, Lee OK, Hadiyati S et al (2019b) Metabolic engineering of the type I methanotroph Methylomonas sp. DH-1 for production of succinate from methane. Metab Eng 54:170–179

    Article  CAS  PubMed  Google Scholar 

  • Nguyen AD, Park JY, Hwang IY et al (2020) Genome-scale evaluation of core one-carbon metabolism in gammaproteobacterial methanotrophs grown on methane and methanol. Metab Eng 57:1–12

    Article  CAS  PubMed  Google Scholar 

  • Öner ET (2013) Microbial production of extracellular polysaccharides from biomass. In: Fang Z (ed) Pretreatment techniques for biofuels and biorefineries. Springer, New York, pp 35–56

    Chapter  Google Scholar 

  • Osawa A, Kaseya Y, Koue N et al (2015) 4-[2-O-11Z-Octadecenoyl-β-glucopyranosyl]-4,4′-diapolycopene-4,4′-dioic acid and 4-[2-O-9Z-hexadecenoyl-β-glucopyranosyl]-4,4′-diapolycopene-4,4′-dioic acid: new C30-carotenoids produced by Methylobacterium. Tetrahedron Lett 56(21):2791–2794

    Article  CAS  Google Scholar 

  • Park S, Hanna ML, Taylor RT et al (1991) Batch cultivation of Methylosinus trichosporiurn OB3b. I: production of soluble methane monooxygenase. Biotechnol Bioeng 38:11

    Article  Google Scholar 

  • Peyraud R, Schneider K, Kiefer P, Massou S, Vorholt JA, Portais J-C (2011) Genome scale reconstruction and system level investigation of the metabolic network of Methylobacterium extorquens AM1. BMC Syst Biol 5:22

    Article  Google Scholar 

  • Pontis HG (2017) Case study: nucleotide sugars. In: Methods for analysis of carbohydrate metabolism in photosynthetic organisms, pp 205–221

    Chapter  Google Scholar 

  • Raisig A, Sandmann G (1999) 4,4-diapophytoene desaturase: catalytic properties of an enzyme from the C30 carotenoid pathway of staphylococcus aureus. J Bacteriol 181(9):4

    Google Scholar 

  • Richter M, Rossello-Mora R (2009) Shifting the genomic gold standard for the prokaryotic species definition. Proc Natl Acad Sci U S A 106(45):19126–19131

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schmidt S, Christen P, Kiefer P, Vorholt JA (2010) Functional investigation of methanol dehydrogenase-like protein XoxF in Methylobacterium extorquens AM1. Microbiology 156(8):2575–2586

    Article  CAS  PubMed  Google Scholar 

  • Sheffield GP (2002) Regulation of methane monooxygenase genes in methanotrophs. Department of biological sciences. University of Warwick, 261

  • Skovran E, Palmer AD, Rountree AM, Good NM, Lidstrom ME (2011) XoxF is required for expression of methanol dehydrogenase in Methylobacterium extorquens AM1. J Bacteriol 193(21):6032-6038

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sonntag F, Kroner C, Lubuta P et al (2015) Engineering Methylobacterium extorquens for de novo synthesis of the sesquiterpenoid alpha-humulene from methanol. Metab Eng 32:82–94

    Article  CAS  PubMed  Google Scholar 

  • Stanley SH, Prior SD, Leak DJ et al (1983) Copper stress underlies the fundamental change in intracellular location of methane monooxygenase in methane oxidizing organisms studies in batch and continuous dultures. Biotechnol Lett 5(7):6

    Article  Google Scholar 

  • Steiger S, Perez-Fons L, Cutting SM, Fraser PD, Sandmann G (2015) Annotation and functional assignment of the genes for the C30 carotenoid pathways from the genomes of two bacteria: Bacillus indicus and Bacillus firmus. Microbiology 161(Pt 1):194–202

    Article  CAS  PubMed  Google Scholar 

  • Stein LY, Yoon S, Semrau JD, Dispirito AA, Crombie A, Murrell JC, Vuilleumier S, Kalyuzhnaya MG, Op den Camp HJ, Bringel F, Bruce D, Cheng JF, Copeland A, Goodwin L, Han S, Hauser L, Jetten MS, Lajus A, Land ML, Lapidus A, Lucas S, Medigue C, Pitluck S, Woyke T, Zeytun A, Klotz MG (2010) Genome sequence of the obligate methanotroph Methylosinus trichosporium strain OB3b. J Bacteriol 192(24):6497–6498

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Strong PJ, Xie S, Clarke WP (2015) Methane as a resource: can the methanotrophs add value? Environ Sci Technol 19:19

    Google Scholar 

  • Tao L, Schenzle A, Odom JM et al (2005) Novel carotenoid oxidase involved in biosynthesis of 4,4′-diapolycopene dialdehyde. Appl Environ Microbiol 71(6):3294–3301

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tavormina PL, Orphan VJ, Kalyuzhnaya MG et al (2011) A novel family of functional operons encoding methane/ammonia monooxygenase-related proteins in gammaproteobacterial methanotrophs. Environ Microbiol Rep 3(1):91–100

    Article  CAS  PubMed  Google Scholar 

  • Trapnell C, Pachter L, Salzberg SL (2009) TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 25(9):1105–1111

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Varghese NJ, Mukherjee S, Ivanova N, Konstantinidis KT, Mavrommatis K, Kyrpides NC, Pati A (2015) Microbial species delineation using whole genome sequences. Nucleic Acids Res 43(14):6761–6771

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • von Mering C, Huynen M, Jaeggi D, Schmidt S, Bork P, Snel B (2003) STRING: a database of predicted functional associations between proteins. Nucleic Acids Res 31(1):258–261

    Article  Google Scholar 

  • Ward N, Larsen O, Sakwa J, Bruseth L, Khouri H, Durkin AS, Dimitrov G, Jiang L, Scanlan D, Kang KH, Lewis M, Nelson KE, Methe B, Wu M, Heidelberg JF, Paulsen IT, Fouts D, Ravel J, Tettelin H, Ren Q, Read T, DeBoy RT, Seshadri R, Salzberg SL, Jensen HB, Birkeland NK, Nelson WC, Dodson RJ, Grindhaug SH, Holt I, Eidhammer I, Jonasen I, Vanaken S, Utterback T, Feldblyum TV, Fraser CM, Lillehaug JR, Eisen JA (2004) Genomic insights into methanotrophy: the complete genome sequence of Methylococcus capsulatus (Bath). PLoS Biol 2(10):e303

    Article  PubMed  PubMed Central  Google Scholar 

  • Whittenbury R, Phillips KC, Wilkinson JF (1970) Enrichment, isolation and some properties of methane-utilizing bacteria. J Gen Microbiol 61:14

    Article  Google Scholar 

  • Yang S, Matsen JB, Konopka M, Green-Saxena A, Clubb J, Sadilek M, Orphan VJ, Beck D, Kalyuzhnaya MG (2013) Global molecular analyses of methane metabolism in methanotrophic Alphaproteobacterium, Methylosinus trichosporium OB3b. Part II. Metabolomics and 13C-labeling study. Front Microbiol 4:70

    Article  PubMed  PubMed Central  Google Scholar 

  • Ye RW, Kelly K (2012) Construction of carotenoid biosynthetic pathways through chromosomal integration in methane-utilizing bacterium Methylomonas sp. strain 16a. Methods Mol Biol 892:185–195

    Article  CAS  PubMed  Google Scholar 

  • Zeng H, Zheng H, Chen H et al (2015) Progress in research on biosynthesis and metabolic engineering of microbial polysaccharides. J Shanxi Univ Technol 31(4):10

    Google Scholar 

Download references

Acknowledgements

We thank the student Jieyu Zhao, Bin Qiao, Guangxiang Yu and Yanyun Guo for their kind help for the study.

Author information

Authors and Affiliations

  1. Tianjin Key Laboratory for Industrial Biological Systems and Bioprocessing Engineering, Tianjin Institute of Industrial Biotechnology, Chinese Academy of Science, Tianjin, 300308, China

    Wei Guo, Ronglin He, Wuxi Chen, Feng Gao & Demao Li

  2. Tianjin Institute of Industrial Biotechnology, Chinese Academy of Science, Tianjin, 300308, China

    Yang Li & Xiaoping Liao

Authors
  1. Wei Guo
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yang Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ronglin He
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Wuxi Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Feng Gao
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Demao Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Xiaoping Liao
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Demao Li or Xiaoping Liao.

Ethics declarations

Conflict of interest

Wei Guo declared that she has no conflicts of interest. Yang Li declared that she has no conflicts of interest. Ronglin He declared that she has no conflicts of interest. Wuxi Chen declared that she has no conflicts of interest. Feng Gao declared that she has no conflicts of interest. Demao Li declared that she has no conflicts of interest. Xiaoping Liao declared that she has no conflicts of interest.

Research involving human rights

This article does not contain any studies with human participants performed by any of the authors.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 187 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Guo, W., Li, Y., He, R. et al. Genome-scale revealing the central metabolic network of the fast growing methanotroph Methylomonas sp. ZR1. World J Microbiol Biotechnol 37, 29 (2021). https://doi.org/10.1007/s11274-021-02995-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11274-021-02995-7

Keywords

Search

Navigation