Abstract
Microbial pigments are considered as one of the main sources of natural types, and the attention to them is increasing in the food and pharmaceutical industries. This study aimed to investigate the effects of pigments extracted from Micrococcus roseus (PEM) on the gene expression of a and b staphylococcal enterotoxins (sea and seb) and their acute toxicity. Real-time PCR was used to study the anti-enterotoxigenic activity of PEM against Staphylococcus aureus at sub-inhibitory concentrations. In addition, the acute toxicity of PEM was evaluated on albino mice through alkaline phosphatase (ALP), aspartate aminotransferas (AST), and alanine aminotransferase (ALT) of liver and its histopathological changes. Based on the results, the expression of sea and seb was decreased in the presence of PEM at sub-inhibitory concentrations. The 2−∆∆CT was measured 0.02 and 0.01 for the expression of sea and seb of S. aureus grown in the MHB containing 16 mg/ml PEM. The results showed that the expression of seb is more sensitive to PEM compared to the expression of sea. After treatment of mice with PEM for two weeks, the condition of mice was normal, and the results of liver enzymatic activities and histopathological changes showed insignificant difference compared to the control sample.
Data availability
The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.
References
Dekanski D, Spremo-Potparević B, Bajić V, Živković L, Topalović D, Sredojević DN, ..., Nedeljković JM (2018) Acute toxicity study in mice of orally administrated TiO2 nanoparticles functionalized with caffeic acid. Food Chem Toxicol 115:42–48
Even S, Charlier C, Nouaille S, Ben Zakour NL, Cretenet M, Cousin FJ, ..., Le Loir Y (2009) Staphylococcus aureus virulence expression is impaired by Lactococcus lactis in mixed cultures. Appl Environ Microbiol 75(13):4459–4472
Fetsch A, Johler S (2018) Staphylococcus aureus as a foodborne pathogen. Curr Clin Microbiol Rep 5(2):88–96
Fischbach MA, Walsh CT (2009) Antibiotics for emerging pathogens. Science 325(5944):1089–1093
Koupaei M, Saderi H, Marashi SMA, Fathizadeh H, Owlia P (2022) Evaluation of the effect of Saccharomyces cerevisiae on the expression of enterotoxin genes in Escherichia coli O157: H7 (EHEC) and Escherichia coli H10407 (ETEC). Microb Pathog 164:105450
Kumari HM, Naidu KA, Vishwanatha S, Narasimhamurthy K, Vijayalakshmi G (2009) Safety evaluation of Monascus purpureus red mould rice in albino rats. Food Chem Toxicol 47(8):1739–1746
Li H, Huang YY, Addo KA, Yu YG, Xiao XL (2022) Effects of cuminaldehyde on toxins production of Staphylococcus aureus and its application in sauced beef. Food Control 137:108960
Liu J, Cai M, Yan H, Fu J, Wu G, Zhao Z, ..., Zeng J (2019) Yunnan Baiyao reduces hospital-acquired pressure ulcers via suppressing virulence gene expression and biofilm formation of Staphylococcus aureus. Int J Med Sci 16(8):1078
Mohana DC, Thippeswamy S, Abhishek RU (2013) Antioxidant, antibacterial, and ultraviolet-protective properties of carotenoids isolated from Micrococcus spp. Radiat Prot Environ 36(4):168–174
Pandit SG, Puttananjaiah MH, Peddha MS, Dhale MA (2020) Safety efficacy and chemical profiling of water-soluble Talaromyces purpureogenus CFRM02 pigment. Food Chem 310:125869
Parsaeimehr M, Akhondzadeh Basti A, Misaghi A, Gandomi H, Jebellijavan A (2015) The effect of Zataria multiflora B oiss. essential oil on gene expression of enterotoxin C in Staphylococcus aureus ATCC 6538. J Food Process Preserv 39(6):1702–1709
Qiu J, Wang D, Xiang H, Feng H, Jiang Y, Xia L, ..., Deng X (2010) Subinhibitory concentrations of thymol reduce enterotoxins A and B and α-hemolysin production in Staphylococcus aureus isolates. PLoS ONE 5(3):e9736
Rostami H, Hamedi H, Yolmeh M (2016) Some biological activities of pigments extracted from Micrococcus roseus (PTCC 1411) and Rhodotorula glutinis (PTCC 5257). Int J Immunopathol Pharmacol 29(4):684–695
Saidi N, Owlia P, Marashi SMA, Saderi H (2019) Inhibitory effect of probiotic yeast Saccharomyces cerevisiae on biofilm formation and expression of α-hemolysin and enterotoxin A genes of Staphylococcus aureus. Iran J Microbiol 11(3):246
Sen T, Barrow CJ, Deshmukh SK (2019) Microbial pigments in the food industry—challenges and the way forward. Front Nutr 6:7
Silva GO, Castro RD, Oliveira LG, Sant’Anna FM, Barbosa CD, Sandes SHC, ..., Souza MR (2020) Viability of Staphylococcus aureus and expression of its toxins (SEC and TSST-1) in cheeses using Lactobacillus rhamnosus D1 or Weissella paramesenteroides GIR16L4 or both as starter cultures. J Dairy Sci 103(5):4100–4108
Smith-Palmer A, Stewart J, Fyfe L (2004) Influence of subinhibitory concentrations of plant essential oils on the production of enterotoxins a and b and α-Toxin by Staphylococcus aureus. J Med Microbiol 53(10):1023–1027
Tambalo FMZ, Garcia JF, Estrellana CD (2022) Safety assessment of a fungal-based red colorant produced by Monascuspurpureus MTCC 25436. Philipp J Sci 151(4):1507–1516
Viçosa GN, Botelho CV, Botta C, Bertolino M, de Carvalho AF, Nero LA, Cocolin L (2019) Impact of co-cultivation with Enterococcus faecalis over growth, enterotoxin production and gene expression of Staphylococcus aureus in broth and fresh cheeses. Int J Food Microbiol 308:108291
Wang H, Cai L, Wang H, Xu X, Zhou G (2019) Influence of protein and vitamin B2 as nutrients of chicken meat on staphylococcal enterotoxin genes expression via virulence regulators. LWT 111:688–693
Yaghoubzadeh Z, Kaboosi H, Peyravii Ghadikolaii F, Safari R, Fattahi E (2020) The half maximal inhibitory concentration (IC50) effect of protein hydrolysates from rainbow trout (Oncorhynchus mykiss) skin on enterotoxin a gene expression in Staphylococcus aureus. Int J Pept Res Ther 26(4):2411–2418
Yolmeh M, Khomeiri M, Ghaemi E (2020) High-efficiency anti-enterotoxigenic activity of Lactobacillus on staphylococcal enterotoxins biosynthesis. LWT 125:109266
Yolmeh M, Khomeiri M, Ghorbani M, Ghaemi E, Ramezanpour SS (2017) High efficiency pigment production from Micrococcus roseus (PTCC 1411) under ultraviolet irradiation. Biocatal Agric Biotechnol 9:156–161
Yolmeh M, Khamiri M, Ghaemi E, RamezanPour SS (2018) Antimicrobial activity of carotenoid pigments extracted from Micrococcus roseus. Modares J Biotechnol 9(4):565–570
Zhang M, Li H, Agyekumwaa AK, Yu Y, Xiao X (2022) Effects of citronellal on growth and enterotoxins production in Staphylococcus aureus ATCC 29213. Toxicon 213:92–98
Funding
This work was supported by Gorgan University of Agricultural Sciences and Natural Resources, Gorgan, Iran.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no conflict of interest.
Additional information
Responsible Editor: Ilana Camargo
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Yolmeh, M., Khomeiri, M., Ghaemi, E. et al. Acute toxicity and anti-enterotoxigenic activity of pigment extracted from Micrococcus roseus. Braz J Microbiol (2024). https://doi.org/10.1007/s42770-024-01316-y
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s42770-024-01316-y