Abstract
Traditional fermented sap beverages from two provinces of Mexico were studied for the isolation of pathogenic bacteria from these beverages. Eight strains of hemolytic Gram positive bacteria, identified as Bacillus pumilus (B. pumilus), were isolated. They showed different antibiotic resistance profiles and tolerances to the simulated gastrointestinal conditions. All the B. pumilus isolated were resistant to at least one antibiotic tested. Regarding the simulated gastrointestinal conditions, strains S1 and S3 were able to tolerate all the conditions. Hemolytic activity has been associated with a health risk and is often considered as a virulence determinant associated with pathogenicity. Therefore, the hemolytic activity along with the ability to tolerate gastrointestinal conditions and the resistance to antibiotics exhibited by B. pumilus strains S1 and S3 could be associated with a health risk for pulque consumers.
Similar content being viewed by others
References
Valadez-Blanco R, Bravo-Villa G, Santos-Sánchez N, Velasco-Almendarez S, Montville T. The artisanal production of pulque, a traditional beverage of the Mexican highlands. Probiotics Antimicrob. Proteins 4: 140–144 (2012)
Backstrand JR, Goodman AH, Allen LH, Pelto GH. Pulque intake during pregnancy and lactation in rural Mexico: Alcohol and child growth from 1 to 57 months. Eur. J. Clin. Nutr. 58: 1626–1634 (2004)
Correa-Ascencio M, Robertson IG, Cabrera-Cortes O, Cabrera-Castro R, Evershed RP. Pulque production from fermented agave sap as a dietary supplement in Prehispanic Mesoamerica. P. Natl. Acad. Sci. USA 111: 14223–14228 (2014)
Gómez-Aldapa CA, Díaz-Cruz CA, Villarruel-López A, Torres-Vitela M, Añorve- Morga J, Rangel-Vargas E, Cerna-Cortes JF, Viqueras-Ramírez JG, Castro-Rosas J. Behavior of Salmonella Typhimurium, Staphylococcus aureus, Listeria monocytogenes, Shigella flexneri and Shigella sonnei during production of pulque, a traditional Mexican beverage. J. Food Protect. 74: 580–587 (2011)
Andersson M, Laukkanen M, Nurmiaho-Lassila EL, Rainey FA, Niemelä SI, Salkinoja-Salonen M. Bacillus thermosphaericus sp.nov. a new thermophilic ureolytic: Bacillus isolated from air. Syst. Appl. Microbiol. 18: 203–220 (1995)
Oguntoyinbo FA, Oni OM. Incidence and characterization of Bacillus cereus isolated from traditional fermented meals in Nigeria. J. Food Protect. 67: 2805–2808 (2004)
Escalante A, López Soto DR, Velázquez Gutiérrez JE, Giles-Gómez M, Bolívar F, López-Munguía A. Pulque, a traditional Mexican alcoholic fermented beverage: Historical, microbiological, and technical aspects. Front. Microbiol. 30: 1026 (2016)
Tamang JP, Watanabe K, Holzapfel, WH. Review: Diversity of microorganisms in global fermented foods and beverages. Front. Microbiol. 7: 377 (2016)
Granum PE, Lund T. Bacillus cereus and its food poisoning toxins. FEMS Microbiol. Lett. 157: 223–228 (1997)
Salkinoja-Salonen MS, Vuorio R, Andersson MA, Kämpfer P, Andersson MC, Honkanen-Buzalski T, Scoging AC. Toxigenic strains of Bacillus licheniformis related to food poisoning. Appl. Environ. Microb. 65: 4637–4645 (1999)
Chilcott CN, Kalmakoff J, Pillai JS. Neurotoxic and haemolytic activity of a protein isolated from Bacillus thuringiensis var. israelensis crystals. FEMS Microbiol. Lett. 25: 259–263 (1984)
Kunst F, Ogasawara N, Moszer I, Albertini AM, Alloni G, Azevedo V, Bertero MG, Bessières P, Bolotin A, Borchert S, et al. The complete genome sequence of the Gram-positive bacterium Bacillus subtilis. Nature 390: 249–256 (1997)
Duc LH, Hong HA, Barbosa TM, Henriques AO, Cutting SM. Characterization of Bacillus probiotics available for human use. Appl. Environ. Microb. 70: 2161–2171 (2004)
González-Vázquez R, Azaola-Espinosa A, Mayorga-Reyes L, Reyes-Nava LA, Shah NP, Rivera-Espinoza Y. Isolation, identification and partial characterization of a Lactobacillus casei strain with bile salt hydrolase activity from pulque. Probiotics Antimicrob. Proteins 7: 242–248 (2015)
Walter J, Hertel C, Tannock GW, Lis CM, Munro K, Hammes WP. Detection of Lactobacillus, Pediococcus, Leuconostoc, and Weissella species in human feces by using group-specific PCR primers and denaturing gradient gel electrophoresis. Appl. Environ. Microb. 67: 2578–2585 (2001)
Kaban G, Kaya M. Identification of lactic acid bacteria and Gram-positive catalase-positive cocci isolated from naturally fermented sausage (sucuk). J. Food Sci. 73: M385–M388 (2008)
Ruiz-Moyano S, Martin A, Benito MJ, Casquete R, Serradilla MJ, Cordoba M de G. Safety and functional aspects of pre-selected lactobacilli for probiotic use in Iberian dry-fermented sausages. Meat Sci. 83: 460–467 (2009)
Cervantes M, Pedroza AM. Pulque: Microbiological charateristics and alcoholic content by Raman spectroscopy. Nova Publicación Científica en Biomédicas 5: 135–146 (2007)
Sutyak KE, Wirawan RE, Aroutcheva AA, Chikindas ML. Isolation of the Bacillus subtilis antimicrobial peptide subtilosin from the dairy product-derived Bacillus amyloliquefaciens. J. Appl. Microbiol. 104: 1067–1074 (2008)
Hartemink R, Domenech VR, Rombouts FM. LAMVAB—A new selective medium for the isolation of lactobacilli from faeces. J. Microbiol. Meth. 29: 77–84 (1997)
Suárez C, Gudiol F. Antibióticos betalactámicos. Enferm. Infecc. Microbiol. Clin. 27: 116–129 (2009)
Martínez JL, Baquero F. Interactions among strategies associated with bacterial infection: Pathogenicity, epidemicity, and antibiotic resistance. Clin. Microbiol. Rev. 15: 647–679 (2002)
Dantas G, Sommer M. How to fight back against antibiotic resistance. Am. Sci. 102: 42–51 (2014)
Brophy PF, Knoop FC. Bacillus pumilus in the induction of clindamycinassociated enterocolitis in guinea pigs. Infect. Immun. 35: 289–295 (1982)
Begley M, Gahan CG, Hill C. The interaction between bacteria and bile. FEMS Microbiol. Rev. 29: 625–651 (2005)
Tena D, Martínez-Torres JA, Pérez-Pomata MT, Sáez-Nieto JA, Rubio V, Bisquert J. Cutaneous infection due to Bacillus pumilus: Report of 3 cases. Clin. Infect. Dis. 44: e40–e42 (2007)
Bottone EJ, Peluso RW. Production by Bacillus pumilus (MSH) of an antifungal compound that is active against Mucoraceae and Aspergillus species: Preliminary report. J. Med. Microbiol. 52: 69–74 (2003)
Hanukoglu A, Danon PN. Endogenous methemoglobinemia associated with diarrheal disease in infancy. J. Pediatr. Gastr. Nutr. 23: 1–7 (1996)
Woollard KJ, Sturgeon S, Chin-Dusting JP, Salem HH, Jackson SP. Erythrocyte hemolysis and hemoglobin oxidation promote ferric chloride-induced vascular injury. J. Biol. Chem. 284: 13110–13118 (2009)
Bielecki J, Youngman P, Connelly P, Portnoy DA. Bacillus subtilis expressing a haemolysin gene from Listeria monocytogenes can grow in mammalian cells. Nature 345: 175–176 (1990)
Matarante A, Baruzzi F, Cocconcelli PS, Morea M. Genotyping and toxigenic potential of Bacillus subtilis and Bacillus pumilus strains occurring in industrial and artisanal cured sausages. Appl. Environ. Microb. 70: 5168–5176 (2004)
Logan NA. Bacillus anthracis, Bacillus cereus, and other aerobic endosporeforming bacteria. pp. 922–52. In: Topley and Wilson’s Microbiology and Microbial Infections. 10th ed. Borriello SP, Murray PR, Funke G (eds). Hodder Arnold and ASM Press, Washington, DC, USA (2005)
Beales N. Adaptation of microorganisms to cold temperatures, weak acid preservatives, low pH, and osmotic stress: A review. Compr. Rev. Food. Sci. F. 3: 1–20 (2004)
Ridlon JM, Kang DJ, Hylemon PB. Bile salt biotransformations by human intestinal bacteria. J. Lipid Res. 47: 241–259 (2006)
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
González-Vázquez, R., Mayorga-Reyes, L., Monroy-López, A. et al. Antibiotic resistance and tolerance to simulated gastrointestinal conditions of eight hemolytic Bacillus pumilus isolated from pulque, a traditional Mexican beverage. Food Sci Biotechnol 26, 447–452 (2017). https://doi.org/10.1007/s10068-017-0061-y
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10068-017-0061-y