Skip to main content
SpringerLink
Log in

Description of Microbacterium luteum sp. nov., Microbacterium cremeum sp. nov., and Microbacterium atlanticum sp. nov., three novel C50 carotenoid producing bacteria

  • Microbial Systematics and Evolutionary Microbiology
  • Published:
Journal of Microbiology Aims and scope Submit manuscript

Abstract

We have identified three Microbacterium strains, A18JL200T, NY27T, and WY121T, that produce C50 carotenoids. Taxonomy shows they represent three novel species. These strains shared < 98.5% 16S rRNA gene sequence identity with each other and were closely related to Microbacterium aquimaris JCM 15625T, Microbacterium yannicii JCM 18959T, Microbacterium ureisolvens CFH S00084T, and Microbacterium hibisci CCTCC AB 2016180T. Digital DNA-DNA hybridization (dDDH) values and average nucleotide identity (ANI) showed differences among the three strains and from their closest relatives, with values ranging from 20.4% to 34.6% and 75.5% to 87.6%, respectively. These values are below the threshold for species discrimination. Both morphology and physiology also differed from those of phylogenetically related Microbacterium species, supporting that they are indeed novel species. These strains produce C50 carotenoids (mainly decaprenoxanthin). Among the three novel species, A18JL200T had the highest total yield in carotenoids (6.1 mg/L or 1.2 mg/g dry cell weight). Unusual dual isoprenoid biosynthetic pathways (methylerythritol phosphate and mevalonate pathways) were annotated for strain A18JL200T. In summary, we found strains of the genus Microbacterium that are potential producers of C50 carotenoids, but their genome has to be investigated further.

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

Similar content being viewed by others

References

  • Asker, D., Awad, T.S., Beppu, T., and Ueda, K. 2018. Rapid and selective screening method for isolation and identification of carotenoid-producing bacteria. In Barreiro, C. and Barredo, J.L. (eds.), Microbial Carotenoids: Methods and Protocols. vol. 1852, pp. 143–170. Humana Press, New York, USA.

    Chapter  Google Scholar 

  • Ausich, R.L. 1997. Commercial opportunities for carotenoid production by biotechnology. Pure Appl. Chem.69, 2169–2174.

    Article  CAS  Google Scholar 

  • Aziz, R.K., Bartels, D., Best, A.A., DeJongh, M., Disz, T., Edwards, R.A., Formsma, K., Gerdes, S., Glass, E.M., Kubal, M., et al. 2008. The RAST Server: rapid annotations using subsystems technology. BMC Genomics9, 75.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Blin, K., Shaw, S., Steinke, K., Villebro, R., Ziemert, N., Lee, S.Y., Medema, M.H., and Weber, T. 2019. antiSMASH 5.0: updates to the secondary metabolite genome mining pipeline. Nucleic Acids Res.47, W81–W87.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cerny, G. 1978. Studies on the aminopeptidase test for the distinction of Gram-negative from Gram-positive bacteria. European J. Appl. Microbiol. Biotechnol.5, 113–122.

    Article  CAS  Google Scholar 

  • Cheng, L., Ming, H., Zhao, Z.L., Ji, W.L., Zhang, L.Y., Li, L., Meng, X., Li, M., Niu, M., and Nie, G.X. 2019. Microbacterium ureisolvens sp. nov., isolated from a Yellow River sample. Int. J. Syst. Evol. Microbiol.69, 560–566.

    Article  CAS  PubMed  Google Scholar 

  • Choi, H.S., Lee, S.Y., Kim, T.Y., and Woo, H.M. 2010. In silico identification of gene amplification targets for improvement of lycopene production. Appl. Environ. Microbiol.76, 3097–3105.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Corretto, E., Antonielli, L., Sessitsch, A., Höfer, C., Puschenreiter, M., Widhalm, S., Swarnalakshmi, K., and Brader, G. 2020. Comparative genomics of Microbacterium species to reveal diversity, potential for secondary metabolites and heavy metal resistance. Front. Microbiol.11, 1869.

    Article  PubMed  PubMed Central  Google Scholar 

  • Courington, D.P. and Goodwin, T.W. 1955. A survey of the pigments of a number of chromogenic marine bacteria, with special reference to the carotenoids. J. Bacteriol.70, 568–571.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Daum, M., Herrmann, S., Wilkinson, B., and Bechthold, A. 2009. Genes and enzymes involved in bacterial isoprenoid biosynthesis. Curr. Opin. Chem. Biol.13, 180–188.

    Article  CAS  PubMed  Google Scholar 

  • Felsenstein, J. 1981. Evolutionary trees from DNA sequences: a maximum likelihood approach. J. Mol. Evol.17, 368–376.

    Article  CAS  PubMed  Google Scholar 

  • Fitch, W.M. 1971. Toward defining the course of evolution: minimum change for a specific tree topology. Syst. Zool.20, 406–416.

    Article  Google Scholar 

  • Giuffrida, D., Sutthiwong, N., Dugo, P., Donato, P., Cacciola, F., Girard-Valenciennes, E., Le Mao, Y., Monnet, C., Fouillaud, M., Caro, Y., et al. 2016. Characterisation of the C50 carotenoids produced by strains of the cheese-ripening bacterium Arthrobacter arilaitensis. Int. Dairy J.55, 10–16.

    Article  CAS  Google Scholar 

  • Gogichaeva, N.V. and Alterman, M.A. 2012. Amino acid analysis by means of MALDI TOF Mass Spectrometry or MALDI TOF/TOF tandem mass spectrometry. In Alterman, M.A. and Hunziker, P. (eds.), Amino Acid Analysis: Methods and Protocols. vol. 828, pp. 121–135. Humana Press, Totowa, New Jersey, USA.

    Chapter  Google Scholar 

  • Goksøyr, A. 2013. Carotenoid sunscreen. US20130078203 A1, USA.

  • He, C., Fan, Y., Liu, G., and Zhang, H. 2008. Isolation and identification of a strain of Aspergillus tubingensis with deoxynivalenol biotransformation capability. Int. J. Mol. Sci.9, 2366–2375.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jin, L., Zhao, Y., Song, W., Duan, L., Jiang, S., Wang, X., Zhao, J., and Xiang, W. 2019. Streptomyces inhibens sp. nov., a novel actinomycete isolated from rhizosphere soil of wheat (Triticum aestivum L.). Int. J. Syst. Evol. Microbiol.69, 688–695.

    Article  CAS  PubMed  Google Scholar 

  • Karojet, S., Kunz, S., and van Dongen, J.T. 2012. Microbacterium yannicii sp. nov., isolated from Arabidopsis thaliana roots. Int. J. Syst. Evol. Microbiol.62, 822–826.

    Article  CAS  PubMed  Google Scholar 

  • Kim, H., Choo, Y.J., Song, J., Lee, J.S., Lee, K.C., and Cho, J.C. 2007. Marinobacterium litorale sp. nov. in the order Oceanospirillales. Int. J. Syst. Evol. Microbiol.57, 1659–1662.

    Article  CAS  PubMed  Google Scholar 

  • Kim, K.K., Lee, K.C., Oh, H.M., and Lee, J.S. 2008. Microbacterium aquimaris sp. nov., isolated from seawater. Int. J. Syst. Evol. Microbiol.58, 1616–1620.

    Article  CAS  PubMed  Google Scholar 

  • Krubasik, P., Kobayashi, M., and Sandmann, G. 2001a. Expression and functional analysis of a gene cluster involved in the synthesis of decaprenoxanthin reveals the mechanisms for C50 carotenoid formation. Eur. J. Biochem.268, 3702–3708.

    Article  CAS  PubMed  Google Scholar 

  • Krubasik, P., Takaichi, S., Maoka, T., Kobayashi, M., Masamoto, K., and Sandmann, G. 2001b. Detailed biosynthetic pathway to decaprenoxanthin diglucoside in Corynebacterium glutamicum and identification of novel intermediates. Arch. Microbiol.176, 217–223.

    Article  CAS  PubMed  Google Scholar 

  • Kumar, S., Stecher, G., Li, M., Knyaz, C., and Tamura, K. 2018. MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol. Biol. Evol.35, 1547–1549.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lange, B.M., Rujan, T., Martin, W., and Croteau, R. 2000. Isoprenoid biosynthesis: the evolution of two ancient and distinct pathways across genomes. Proc. Natl. Acad. Sci.97, 13172–13177.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee, I., Kim, Y.O., Park, S.C., and Chun, J. 2016. OrthoANI: an improved algorithm and software for calculating average nucleotide identity. Int. J. Syst. Evol. Microbiol.66, 1100–1103.

    Article  CAS  PubMed  Google Scholar 

  • Leifson, E. 1960. Atlas of bacterial flagellation. Academic Press, New York, USA.

    Book  Google Scholar 

  • Liu, N., Liu, B., Wang, G., Soong, Y.H.V., Tao, Y., Liu, W., and Xie, D. 2020. Lycopene production from glucose, fatty acid and waste cooking oil by metabolically engineered Escherichia coli. Biochem. Eng. J.155, 107488.

    Article  CAS  Google Scholar 

  • Ludwig, W. 2007. Nucleic acid techniques in bacterial systematics and identification. Int. J. Food Microbiol.120, 225–236.

    Article  CAS  PubMed  Google Scholar 

  • Mata-Gómez, L.C., Montañez, J.C., Méndez-Zavala, A., and Aguilar, C.N. 2014. Biotechnological production of carotenoids by yeasts: an overview. Microb. Cell Fact.13, 12.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Meddeb-Mouelhi, F., Moisan, J.K., Bergeron, J., Daoust, B., and Beauregard, M. 2016. Structural characterization of a novel antioxidant pigment produced by a photochromogenic Microbacterium oxydans strain. Appl. Biochem. Biotechnol.180, 1286–1300.

    Article  CAS  PubMed  Google Scholar 

  • Meier-Kolthoff, J.P., Auch, A.F., Klenk, H.P., and Göker, M. 2013. Genome sequence-based species delimitation with confidence intervals and improved distance functions. BMC Bioinformatics14, 60.

    Article  PubMed  PubMed Central  Google Scholar 

  • Minnikin, D.E., Patel, P.V., Alshamaony, L., and Goodfellow, M. 1977. Polar lipid composition in the classification of Nocardia and related bacteria. Int. J. Syst. Evol. Microbiol.27, 104–117.

    CAS  Google Scholar 

  • Montero-Lobato, Z., Ramos-Merchante, A., Fuentes, J.L., Sayago, A., Fernández-Recamales, Á., Martínez-Espinosa, R.M., Vega, J.M., Vílchez, C., and Garbayo, I. 2018. Optimization of growth and carotenoid production by Haloferax mediterranei using response surface methodology. Mar. Drugs16, 372.

    Article  CAS  PubMed Central  Google Scholar 

  • Na, S.I., Kim, Y.O., Yoon, S.H., Ha, S.M., Baek, I., and Chun, J. 2018. UBCG: up-to-date bacterial core gene set and pipeline for phylogenomic tree reconstruction. J. Microbiol.56, 280–285.

    Article  CAS  PubMed  Google Scholar 

  • Netzer, R., Stafsnes, M.H., Andreassen, T., Goksøyr, A., Bruheim, P., and Brautaset, T. 2010. Biosynthetic pathway for γ-cyclic Sarcinaxanthin in Micrococcus luteus heterologous expression and evidence for diverse and multiple catalytic functions of C50 carotenoid cyclases. J. Bacteriol.192, 5688–5699.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Niu, S., Zhou, T.T., Xie, C.L., Zhang, G.Y., and Yang, X.W. 2017. Microindolinone A, a novel 4,5,6,7-tetrahydroindole, from the deep-sea-derived actinomycete Microbacterium sp. MCCC 1A11207. Mar. Drugs15, 230.

    Article  PubMed Central  CAS  Google Scholar 

  • Osawa, A., Ishii, Y., Sasamura, N., Morita, M., Kasai, H., Maoka, T., and Shindo, K. 2010. Characterization and antioxidative activities of rare C50 carotenoids sarcinaxanthin, sarcinaxanthin monoglucoside, and sarcinaxanthin diglucoside-obtained from Micrococcus yunnanensis. J. Oleo Sci.59, 653–659.

    Article  CAS  PubMed  Google Scholar 

  • Park, S.Y., Binkley, R.M., Kim, W.J., Lee, M.H., and Lee, S.Y. 2018. Metabolic engineering of Escherichia coli for high-level astaxanthin production with high productivity. Metab. Eng.49, 105–115.

    Article  CAS  PubMed  Google Scholar 

  • Saitou, N. and Nei, M. 1987. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol.4, 406–425.

    CAS  PubMed  Google Scholar 

  • Sasidharan, P., Raja, R., Karthik, C., Ranandkumar, S., and Indra Arulselvi, P. 2013. Isolation and characterization of yellow pigment producing Exiguobacterium sps. J. Biochem. Tech.4, 632–635.

    CAS  Google Scholar 

  • Sasser, M. 1990. Identification of bacteria by gas chromatography of cellular fatty acids. MIDI Technical Note 101. MIDI Inc., Newark, Delaware, USA.

    Google Scholar 

  • Savi, D.C., Shaaban, K.A., Gos, F.M.W., Thorson, J.S., Glienke, C., and Rohr, J. 2019. Secondary metabolites produced by Microbacterium sp. LGMB471 with antifungal activity against the phytopathogen Phyllosticta citricarpa. Folia Microbiol.64, 453–460.

    Article  CAS  Google Scholar 

  • Schippers, A., Bosecker, K., Spröer, C., and Schumann, P. 2005. Microbacterium oleivorans sp. nov. and Microbacterium hydrocarbonoxydans sp. nov., novel crude-oil-degrading Gram-positive bacteria. Int. J. Syst. Evol. Microbiol.55, 655–660.

    Article  CAS  PubMed  Google Scholar 

  • Schleifer, K.H. and Kandler, O. 1972. Peptidoglycan types of bacterial cell walls and their taxonomic implications. Bacteriol. Rev.36, 407–477.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schrader, J. and Bohlmann, J. 2015. Biotechnology of isoprenoids. Springer, Cham, Switzerland.

    Book  Google Scholar 

  • Schumann, P. 2011. 5 — Peptidoglycan Structure. In Rainey, F. and Oren, A. (eds.), Methods in Microbiology, vol. 38, pp. 101–129. Academic Press, London, United Kingdom.

    Google Scholar 

  • Seto, H., Watanabe, H., and Furihata, K. 1996. Simultaneous operation of the mevalonate and non-mevalonate pathways in the biosynthesis of isopentenly diphosphate in Streptomyces aeriouvifer. Tetrahedron Lett.37, 7979–7982.

    Article  CAS  Google Scholar 

  • Takeuchi, M. and Hatano, K. 1998. Union of the genera Microbacterium Orla-Jensen and Aureobacterium Collins et al. in a redefined genus Microbacterium. Int. J. Syst. Evol. Microbiol.48, 739–747.

    CAS  Google Scholar 

  • Taniguchi, H., Henke, N.A., Heider, S.A.E., and Wendisch, V.F. 2017. Overexpression of the primary sigma factor gene sigA improved carotenoid production by Corynebacterium glutamicum application to production of β-carotene and the non-native linear C50 carotenoid bisanhydrobacterioruberin. Metab. Eng. Commun.4, 1–11.

    Article  PubMed  PubMed Central  Google Scholar 

  • van Belkum, A. and Hermans, P.W. 2001. BOX PCR fingerprinting for molecular typing of Streptococcus pneumoniae. In Gillespie S.H. (ed.), Antibiotic Resistence. Methods in Molecular Medicine, vol. 48, pp. 159–168. Humana Press. Totowa, New Jersey, USA.

    Google Scholar 

  • van der Weele, C.M., Spollen, W.G., Sharp, R.E., and Baskin, T.I. 2000. Growth of Arabidopsis thaliana seedlings under water deficit studied by control of water potential in nutrient-agar media. J. Exp. Bot.51, 1555–1562.

    Article  CAS  PubMed  Google Scholar 

  • Venil, C.K., Zakaria, Z.A., and Ahmad, W.A. 2013. Bacterial pigments and their applications. Process Biochem.48, 1065–1079.

    Article  CAS  Google Scholar 

  • Vila, E., Hornero-Méndez, D., Azziz, G., Lareo, C., and Saravia, V. 2019. Carotenoids from heterotrophic bacteria isolated from Fildes Peninsula, King George Island, Antarctica. Biotechnol. Rep.21, e00306.

    Article  Google Scholar 

  • Xie, F., Pei, S., Lin, X., Tian, Y., and Zhang, G. 2021. A rapid and efficient method for the extraction and identification of menaquinones from Actinomycetes in wet biomass. BMC Microbiol.21, 175.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yan, Z.F., Lin, P., Won, K.H., Yang, J.E., Li, C.T., Kook, M.C., Wang, Q.J., and Yi, T.H. 2017. Microbacterium hibisci sp. nov., isolated from rhizosphere of mugunghwa (Hibiscus syriacus L.). Int. J. Syst. Evol. Microbiol.67, 3564–3569.

    Article  CAS  PubMed  Google Scholar 

  • Yang, J. and Guo, L. 2014. Biosynthesis of β-carotene in engineered E. coli using the MEP and MVA pathways. Microb. Cell Fact.13, 160.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yoon, S.H., Ha, S.M., Kwon, S., Lim, J., Kim, Y., Seo, H., and Chun, J. 2017. Introducing EzBioCloud: a taxonomically united database of 16S rRNA gene sequences and whole-genome assemblies. Int. J. Syst. Evol. Microbiol.67, 1613–1617.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This work was supported by China Ocean Mineral Resources R&amp;D Association (COMRA) Program (No. DY135-B2-01) and the Scientific Research Foundation of Third Institute of Oceanography, MNR (No. 2019011).

All authors have contributed to the creation of this manuscript for important intellectual content and read and approved the final manuscript.

Author information

Authors and Affiliations

  1. Key Laboratory of the Ministry of Education for Coastal and Wetland Ecosystems, School of Life Sciences, Xiamen University, Xiamen, 361102, Fujian, P. R. China

    Fuquan Xie & Yun Tian

  2. Key Laboratory of Marine Biogenetic Resources, Third Institute of Oceanography, Ministry of Natural Resources, Xiamen, 361005, Fujian, P. R. China

    Fuquan Xie, Shengxiang Pei, Li Jiang & Gaiyun Zhang

  3. Engineering Innovation Center for the Development and Utilization of Marine Bioresources, Third Institute of Oceanography, Ministry of Natural Resources, Xiamen, 361005, Fujian, P. R. China

    Siwen Niu

  4. Analysis and Test Center, Third Institute of Oceanography, Ministry of Natural Resources, Xiamen, 361005, Fujian, P. R. China

    Xihuang Lin

Authors
  1. Fuquan Xie
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Siwen Niu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Xihuang Lin
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Shengxiang Pei
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Li Jiang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Yun Tian
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Gaiyun Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Gaiyun Zhang.

Ethics declarations

We declare there is no conflict of interest.

Additional information

Supplemental material for this article may be found at http://www.springerlink.com/content/120956.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Xie, F., Niu, S., Lin, X. et al. Description of Microbacterium luteum sp. nov., Microbacterium cremeum sp. nov., and Microbacterium atlanticum sp. nov., three novel C50 carotenoid producing bacteria. J Microbiol. 59, 886–897 (2021). https://doi.org/10.1007/s12275-021-1186-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12275-021-1186-5

Keywords

Search

Navigation