Abstract—
The article presents the results of a study of some adaptive properties of a bacterial isolate from wheat bran, identified by the 16S rRNA gene as an Arthrobacter agilis strain. According to the literature data, A. agilis does not belong to the dominant bacterial species of wheat microbial associations and activates growth at low ambient temperatures. The studied A. agilis strain showed poor growth in a microbial consortium when an aqueous suspension of wheat bran, partially fermented at 28 ± 1°C by the native microbiota, was plated on a dense MPA medium and produced the pigment after three weeks of storage at 4 ± 1°C. Moderate growth of bacteria without increased pigmentation was observed during its subsequent transfer after low-temperature storage on agar media containing carbohydrates and nitrogen compounds, mineral salts, and vitamins that were more easily utilized than native bran. The growth of colonies upon plating on such media increased in the series: thermally fermented wheat bran → HMF agar → LB (without salt). It was revealed that the A. agilis strain, which was not typical of the wheat bran microflora, under the influence of osmotic and/or temperature shock (in response to a sharp change in the NaCl concentration and/or a difference in ambient temperatures) produced pigments both in agar and liquid cultures. According to the results of spectral analysis, the pigment was assigned to carotenoids and tentatively identified as bacterioruberin. Quantitative evaluation showed that, under stress conditions during submerged cultivation, the studied strain A. agilis wb28 was able to synthesize the pigment at the level of 52.8 mg/L (17.2 mg/g biomass).
Similar content being viewed by others
REFERENCES
Afra, S., Makhdoumi, A., Matin, M.M., and Feizy, J., A novel red pigment from marine Arthrobacter sp. G20 with specific anticancer activity, J. Appl. Microbiol., 2017, vol. 123, pp. 1228–1236.
Bergey’s Manual of Systematics of Archaea and Bacteria, New York: Wiley, 2015. ISBN: 978-1-118-96060-8.
Bertani, G., Lysogeny at mid-twentieth century: P1, P2, and other experimental systems, J. Bacteriol., 2004, vol. 186, no. 3, pp. 595–600. ISBN 978-0-19-104072-6.
Davidson A. and Jaine, T., The Oxford Companionto Food, Oxford: Oxford Univ. Press, 2014.
Zhang D.-C., Schumann P., Liu H.-C., Xin Y.-H., Zhou Y.-G., Schinner F., Margesin R., Arthrobacter alpinus sp. nov., a psychrophilic bacterium isolated from alpine soil // Int. J. Syst. Evol. Microbiol. 2010, vol. 60, pp. 2149–2153.
Flegler, A. and Lipski, A., Engineered CRISPR/Cas9 system for transcriptional gene silencing in Arthrobacter species indicates bacterioruberin is indispensable for growth at low temperatures, Curr. Microbiol., 2022a, vol. 79, p. 199.
Flegler, A. and Lipski, A., The C50 carotenoid bacterioruberin regulates membrane fluidity in pink-pigmented Arthrobacter species, Curr. Microbiol., 2022b, vol. 204, p. 70.
Fong, N., Burgess, M., Barrow, K., and Glenn, D., Carotenoid accumulation in the psychrotrophic bacterium Arthrobacter agilis in response to thermal and salt stress, Appl. Microbiol. Biotechnol., 2001, vol. 56, no. 5, pp. 750–756.
Hezayen, F.F., Tindall, B.J., Steinbüchel, A., and Rehm, B.H.A., Characterization of a novel halophilic archaeon, Halobiformahaloterrestris gen. nov., sp. nov., and transfer of Natronobacterium nitratireducens to Halobiforma nitratireducens comb. nov., Int. J. Syst. Evol. Microbiol. 2002, vol. 52, pp. 2272–2280.
Hu, Q.-W., Chu, X., Xiao, M., Li, C.-T., Yan, Z.-F., Hozzein, W.N., Kim, C.-J., Zhi, X.-Y., and Li, W.-J., Arthrobacter deserti sp. nov., isolated from a desert soil sample, Int. J. Syst. Evol. Microbiol., 2016, vol. 66, no. 5, pp. 2035–2040.
Jones, D. and Keddie, R.M., The Genus Arthrobacter, in The Prokaryotes, Dworkin, M., Falkow, S., Rosenberg, E., Schleifer, K.H., and Stackebrandt, E., Eds., New York: Springer, 2006. https://doi.org/10.1007/0-387-30743-5_36
Kim, S., Park, H., and Choi, J., Cloning and characterization of cold-adapted α-amylase from Antarctic Arthrobacter agilis, Appl. Biochem. Biotechnol., 2017, vol. 181, no. 3, pp. 1048–1059.
Kumar, R., Singh, D., Swarnkar, M.K., Singh, A.K., and Kumar, S., Complete genome sequence of Arthrobacter alpinus ERGS4:06, a yellow pigmented bacterium tolerant to cold and radiations isolated from Sikkim Himalaya, J. Biotechnol., 2016, vol. 220, pp. 86–87.
Margesin, R., Schumann, P., Sproer, C., and Gounot, A.M., Arthrobacter psychrophenolicus sp. nov., isolated from an alpine ice cave, Int. J. Syst. Evol. Microbiol., 2004, vol. 54, pp. 2067−2072.
Ozdal, M., Ozdal, O.G., Gürkök, S., Statistical optimization of β-carotene production by Arthrobacter agilis A17 using response surface methodology and Box-Behnken designm. II. Int. Conf. on Advances in Natural and Applied Sciences. 18–21 April 2017, Antalya, Turkey. Eds. Akdemir A.O., Ekinci A., Han I., Set E., Dadasoglu F., Karagoz K., Oztekin A., AIP Conference Proceedings, 2017, vol. 1833, Iss. 1, id.020101, publ. Apr. 25, 2017. ISBN: 978-0-7354-1503-4.
Ozdal, M., Ozdal, O.G., Sezen, A., Algur, O.F., Kurbanoglu, E.B., Continuous production of indole-3-acetic acid by immobilized cells of Arthrobacter agilis, 3 Biotech. 2017, vol. 7, art. 23, pp. 1‒6.
Nikaido H. The Limitations of LB medium. Small things considered, The Microbe Blog, ASM. http://schaechter.asmblog.org/schaechter/2009/11/the-limitations-of-lb-medium.html. Archive copy of November 12, 2020 on Wayback Machine.
Reddy, G.S.N., Prakash, J.S.S., Matsumoto, G.I., Stackebrandt, E., and Shivaji, S., Arthrobacter roseus sp. nov., a psychrophilic bacterium isolated from an antarctic cyanobacterial mat sample., Int. J. Syst. Evol. Microbiol., 2002, vol. 52, no. 3, pp. 1017–1021.
Sahli, K., Gomri, M.A., Esclapez, J., Gómez-Villegas, P., Bonete, M.J., León, R., and Kharroub, K., Characterization and biological activities of carotenoids produced by three haloarchaeal strains isolated from Algerian salt lakes, Arch. Microbiol., 2022, vol. 204, no. 6, p. 6. https://doi.org/10.1007/s00203-021-02611-0
Saini, R.K. and Keum, Y.S., Microbial platforms to produce commercially vital carotenoids at industrial scale: an updated review of critical issues, J. Ind. Microbiol. Biotechnol., 2019, vol. 46, pp. 657–674.
Singh, R.N., Gaba, S., Yadav, A.N., Gaur, P., Kaushik, R., and Saxena, A.K., First high-quality draft genome sequence of a plant growth promoting and cold active enzyme producing psychrotrophic Arthrobacter agilis strain L77, Stand. Genomic Sci., 2016, no. 1, pp. 1–9.
Tamura, K., Peterson, D., Peterson, N., and Stecher, G., MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony method, Mol. Biol. Evol., 2011, vol. 28, no. 10, pp. 2731–2739.
Velázquez-Becerra, C., Macías-Rodríguez, L.I., López-Bucio, J., and Flores-Cortez I., The rhizobacterium Arthrobacter agilis produces dimethylhexadecylamine, a compound that inhibits growth of phytopathogenic fungi in vitro, Protoplasma, 2013, no. 1, pp. 100−112.
Weisburg, W.G., Barns, S.M., Pelletier, D.A., and Lane, D.J., 16S ribosomal DNA amplification for phylogenetic study, J. Bacteriol., 1991, vol. 173, no. 2, pp. 697–703.
Yang, L.-L., Liu, H.-C., Liu, Q., and Xin, Y.-H., Arthrobacter cheniae and Arthrobacter frigidicola sp. nov., isolated from a glacier, Int. J. Syst, Evol. Microbiol., 2021, vol. 71, no. 12, p. 005177.
Yastrebova, O.V. and Plotnikova, E.G., Halotolerant bacterial degradersof polycyclic aromatic hydrocarbons of the genus Arthrobacter, Vestn. Perm. Univ., 2007, vol. 5, no. 10, pp. 100–106.
Ye, J.J., Liu, S.-W., Lu, Q.-P., Cheema, M. T., Abbas, M., Sajid, I., Huang, D.-L., and Sung, C.-H., Arthrobacter mobilis sp. nov., a novel actinobacterium isolated from Cholistan desert soil, Int. J. Syst. Evol. Microbiol., 2020, vol. 70, no. 10, pp. 5445–5452.
Zalazar, L., Pagola, P., Miró, M.V., Churio, M.S., Cerletti, M., Martínez, C., Iniest-Cuerda, M., Soler, A.J., Cesari, A., and De Castro, R., Bacterioruberin extracts from a genetically modified hyperpigmented Haloferax volcanii strain: antioxidant activity and bioactive properties on sperm cells, J. Appl. Microbiol., 2018, vol. 126, pp. 796–810.
Zhang, D.-C., Schumann, P., Liu, H.-C., Xin, Y.-H., Zhou, Y.-G., Schinner, F., and Margesin, R., Arthrobacter alpinus sp. nov., a psychrophilic bacterium isolated from alpine soil, Int. J. Syst. Evol. Microbiol., 2010, vol. 60, pp. 2149–2153.
ACKNOWLEDGMENTS
The authors are grateful to the workers of the All-Russian Research Institute for Agricultural Microbiology for their help in microbial identification using the 16S rRNA gene sequences.
Funding
Research on the topic FGUS-2022-0003 was carried out within the framework of the State Assignment no. 075-01190-22-00 for the All‑Russia Research Institute for Food Additives—Branch of Gorbatov Federal Research Center for Food Systems, Russian Academy of Sciences.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
The authors declare that they have no conflicts of interest. This article does not contain any studies involving animals or human participants performed by any of the authors.
Additional information
Translated by P. Sigalevich
Rights and permissions
About this article
Cite this article
Sharova, N.Y., Prichepa, A.O., Sverdlova, O.P. et al. Adaptive Properties of Arthrobacter agilis Strain wb28 Isolated from Wheat Bran. Microbiology 92, 666–674 (2023). https://doi.org/10.1134/S0026261723600684
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1134/S0026261723600684