Physiological characteristics of Bacillus strains originated from dairy products and their impacts on rheological properties of pasteurised yoghurt
Hui Tian
School of Life Sciences and Engineering, Lanzhou University of Technology, Lanzhou, 730050 Gansu, China
Joint Lab of Collaborative Innovation Center for Supporting Technology of Northwest Low-Carbon Towns, Lanzhou, 730050 Gansu, China
Contribution: Conceptualization, Data curation, Writing - review & editing
Search for more papers by this authorChunlan Shi
School of Life Sciences and Engineering, Lanzhou University of Technology, Lanzhou, 730050 Gansu, China
Contribution: Investigation, Methodology, Data curation, Writing - original draft
Search for more papers by this authorZhuo Ma
School of Life Sciences and Engineering, Lanzhou University of Technology, Lanzhou, 730050 Gansu, China
Contribution: Data curation, Investigation, Validation
Search for more papers by this authorHuiyun Zhou
School of Life Sciences and Engineering, Lanzhou University of Technology, Lanzhou, 730050 Gansu, China
Contribution: Investigation, Methodology
Search for more papers by this authorCorresponding Author
Wenguang Fan
School of Life Sciences and Engineering, Lanzhou University of Technology, Lanzhou, 730050 Gansu, China
Author for correspondence. E-mail: [email protected]; [email protected]
Contribution: Supervision, Project administration
Search for more papers by this authorWenwei Zhang
College of Food Science and Engineering, Gansu Agricultural University, Lanzhou, 730070 Gansu, China
Contribution: Methodology, Validation
Search for more papers by this authorYonggang Wang
College of Food Science and Engineering, Gansu Agricultural University, Lanzhou, 730070 Gansu, China
Contribution: Conceptualization, Validation
Search for more papers by this authorCorresponding Author
Haiwei Ren
School of Life Sciences and Engineering, Lanzhou University of Technology, Lanzhou, 730050 Gansu, China
Joint Lab of Collaborative Innovation Center for Supporting Technology of Northwest Low-Carbon Towns, Lanzhou, 730050 Gansu, China
Author for correspondence. E-mail: [email protected]; [email protected]
Contribution: Conceptualization, Validation
Search for more papers by this authorJinping Li
Joint Lab of Collaborative Innovation Center for Supporting Technology of Northwest Low-Carbon Towns, Lanzhou, 730050 Gansu, China
Contribution: Validation
Search for more papers by this authorXia Cai
School of Life Sciences and Engineering, Lanzhou University of Technology, Lanzhou, 730050 Gansu, China
Contribution: Methodology
Search for more papers by this authorRuiyun Wang
Gansu Qimu Dairy Co., Ltd (Jiuquan Iron and Steel Group), Jiayuguan, 735100 Gansu, China
Contribution: Validation
Search for more papers by this authorHui Tian
School of Life Sciences and Engineering, Lanzhou University of Technology, Lanzhou, 730050 Gansu, China
Joint Lab of Collaborative Innovation Center for Supporting Technology of Northwest Low-Carbon Towns, Lanzhou, 730050 Gansu, China
Contribution: Conceptualization, Data curation, Writing - review & editing
Search for more papers by this authorChunlan Shi
School of Life Sciences and Engineering, Lanzhou University of Technology, Lanzhou, 730050 Gansu, China
Contribution: Investigation, Methodology, Data curation, Writing - original draft
Search for more papers by this authorZhuo Ma
School of Life Sciences and Engineering, Lanzhou University of Technology, Lanzhou, 730050 Gansu, China
Contribution: Data curation, Investigation, Validation
Search for more papers by this authorHuiyun Zhou
School of Life Sciences and Engineering, Lanzhou University of Technology, Lanzhou, 730050 Gansu, China
Contribution: Investigation, Methodology
Search for more papers by this authorCorresponding Author
Wenguang Fan
School of Life Sciences and Engineering, Lanzhou University of Technology, Lanzhou, 730050 Gansu, China
Author for correspondence. E-mail: [email protected]; [email protected]
Contribution: Supervision, Project administration
Search for more papers by this authorWenwei Zhang
College of Food Science and Engineering, Gansu Agricultural University, Lanzhou, 730070 Gansu, China
Contribution: Methodology, Validation
Search for more papers by this authorYonggang Wang
College of Food Science and Engineering, Gansu Agricultural University, Lanzhou, 730070 Gansu, China
Contribution: Conceptualization, Validation
Search for more papers by this authorCorresponding Author
Haiwei Ren
School of Life Sciences and Engineering, Lanzhou University of Technology, Lanzhou, 730050 Gansu, China
Joint Lab of Collaborative Innovation Center for Supporting Technology of Northwest Low-Carbon Towns, Lanzhou, 730050 Gansu, China
Author for correspondence. E-mail: [email protected]; [email protected]
Contribution: Conceptualization, Validation
Search for more papers by this authorJinping Li
Joint Lab of Collaborative Innovation Center for Supporting Technology of Northwest Low-Carbon Towns, Lanzhou, 730050 Gansu, China
Contribution: Validation
Search for more papers by this authorXia Cai
School of Life Sciences and Engineering, Lanzhou University of Technology, Lanzhou, 730050 Gansu, China
Contribution: Methodology
Search for more papers by this authorRuiyun Wang
Gansu Qimu Dairy Co., Ltd (Jiuquan Iron and Steel Group), Jiayuguan, 735100 Gansu, China
Contribution: Validation
Search for more papers by this authorAbstract
Due to the strong stress resistance, causing food spoilage and toxin production of spore-forming Bacillus species, their presence will be detrimental to the quality assurance of dairy products. Impacts of five Bacillus strains (Bacillus licheniformis H1, B. licheniformis H2, B. subtilis Z2, B. cereus Z6-1 and B. cereus Z6-2) originated from dairy products on the quality of pasteurised yoghurt were investigated. Physiological characteristics of the strains, including growth, acid production, proteolysis, amylase production, extracellular polysaccharide and biofilm formation, were analysed. Additionally, changes in Bacillus-contaminated pasteurised yoghurt during a 60-day incubation at 28°C were observed. Physiological characteristics of the five Bacillus strains were strongly strain-specific. Both B. cereus strains had the highest growth rate and acid production in Brian Heart Infusion broth and the strongest proteolytic ability in skimmed milk. Bacillus subtilis Z2 exhibited the highest amylase activity, while the highest yields of extracellular polysaccharides and biofilm were obtained from B. cereus Z6-2 and B. licheniformis H2. The acidic environment (about pH 4.2–4.4) was not suitable for the growth of Bacilli, as the low survival rate after inoculation and the slow growth. Yoghurt contaminated with B. licheniformis H1 showed strong proteolytic activity, resulting in a gel with relatively low elasticity. Yoghurt containing H2 exhibited a high amylase activity, leading to the formation of many interspersed holes. The Z2 strain had the strongest effect on the rheological properties of yoghurt, resulting in the lowest viscoelasticity. Protease from Bacillus strains mainly interferes with the thickness of the protein matrix in the yoghurt, while amylase mainly affects the size of holes in the gel. The residual Bacillus strains may adversely affect the rheological properties of pasteurised yoghurt, particularly in products with a long shelf life.
CONFLICT OF INTEREST
The authors have no conflicts of interest to declare.
Open Research
DATA AVAILABILITY STATEMENT
Data can be made available upon request.
REFERENCES
- Afonso A C, Gomes I B, Saavedra M J, Giaouris E, Simões L C and Simões M (2021) Bacterial coaggregation in aquatic systems. Water Research 196 117037.
- Afrisham S, Badoei-Dalfard A, Namaki-Shoushtari A and Karami Z (2016) Characterization of a thermostable, CaCl2-activated and raw-starch hydrolyzing alpha-amylase from Bacillus licheniformis AT70: production under solid state fermentation by utilizing agricultural wastes. Journal of Molecular Catalysis B: Enzymatic 132 98–106.
- Burgess S A, Lindsay D and Flint S H (2010) Thermophilic bacilli and their importance in dairy processing. International Journal of Food Microbiology 144 215–225.
- Carlin F (2011) Origin of bacterial spores contaminating foods. Food Microbiology 28 177–182.
- Chen J, Cui Y, Shi W, Ma Y and Zhang S (2023) The interaction between wheat starch and pectin with different esterification degree and its influence on the properties of wheat starch-pectin gel. Food Hydrocolloids 145 109062.
- Cho W I and Chung M S (2020) Bacillusspores: a review of their properties and inactivation processing technologies. Food Science and Biotechnology 29 1447–1461.
- De Jonghe V, Coorevits A, De Block J, Van Coillie E, Grijspeerdt K, Herman L, De Vos P and Heyndrickx M (2010) Toxinogenic and spoilage potential of aerobic spore-formers isolated from raw milk. International Journal of Food Microbiology 136 318–325.
- Etesami H, Jeong B R and Glick B R (2023) Biocontrol of plant diseases by Bacillus spp. Physiological and Molecular Plant Pathology 126 102048.
- Fincan S A, Özdemir S, Karakaya A, Enez B, Mustafov S D, Ulutaş M S and Şen F (2021) Purification and characterization of thermostable α-amylase produced from Bacillus licheniformis So-B3 and its potential in hydrolyzing raw starch. Life Sciences 264 118639.
- Freitas F, Alves V D and Reis M A M (2011) Advances in bacterial exopolysaccharides: from production to biotechnological applications. Trends in Biotechnology 29 388–398.
- Gopinath S C B, Anbu P, Arshad M K M, Lakshmipriya T, Voon C H, Hashim U and Chinni S V (2017) Biotechnological processes in microbial amylase production. BioMed Research International 2017. 2017 1–9.
- He J, Han Y, Liu M, Wang Y, Yang Y and Yang X (2019) Effect of 2 types of resistant starches on the quality of yogurt. Journal of Dairy Science 102 3956–3964.
- Heyndrickx M and Scheldeman P (2008) Bacilli associated with spoilage in dairy products and other food. In Applications and Systematics of Bacillus and Relatives, pp. 64–82. R Berkeley, M Heyndrickx, N Logan and P De Vos, eds. Hoboken, NJ: Blackwell Publishing.
10.1002/9780470696743.ch6 Google Scholar
- Homaei A and Qeshmi F I (2022) Purification and characterization of a robust thermostable protease isolated from Bacillus subtilis strain HR02 as an extremozyme. Journal of Applied Microbiology 133 2779–2789.
- Hu X L, Yuan X, He N S, Zhuang T Z, Wu P and Zhang G M (2019) Expression of Bacillus licheniformis α-amylase in Pichia pastoris without antibiotics-resistant gene and effects of glycosylation on the enzymic thermostability. 3 Biotech 9 427.
- Kos B, Suskovic J, Vukovic S, Simpraga M, Frece J and Matosic S (2003) Adhesion and aggregation ability of probiotic strain Lactobacillus acidophilus M92. Journal of Applied Microbiology 94 981–987.
- Li H, Sun J, Mu x et al. (2023) Impacts of cold-extrusion whey protein isolate synergized with inulin on physicochemical characteristics of fermented milk. Food Bioscience 54 102873.
- Lima F T and Souza V M A (2023) A large comparison of normalization methods on time series. Big Data Research 34 100407.
- Lin Y, Briandet R and Kovács Á T (2022) Bacillus cereus sensu lato biofilm formation and its ecological importance. Biofilms 4 100070.
- Ludikhuyze L R, Van den Broeck I, Weemaes C A and Hendrickx M E (1997) Kinetic parameters for pressure−temperature inactivation of Bacillus subtilis α-amylase under dynamic conditions. Biotechnology Progress 13 617–623.
- Machado S G, Baglinière F, Marchand S, Van Coillie E, Vanetti M C D, De Block J and Heyndrickx M (2017) The biodiversity of the microbiota producing heat-resistant enzymes responsible for spoilage in processed bovine milk and dairy products. Frontiers in Microbiology 8 302.
- Mehta D S, Metzger L E, Hassan A N, Nelson B K and Patel H A (2019) The ability of spore formers to degrade milk proteins, fat, phospholipids, common stabilizers, and exopolysaccharides. Journal of Dairy Science 102 10799–10813.
- Meng L, Zhang R R, Dong L, Hu H Y, Liu H M, Zheng N, Wang J Q and Cheng J B (2022) Characterization and spoilage potential of Bacillus cereus isolated from farm environment and raw milk. Frontiers in Microbiology 13 940611.
- Miller R A, Kent D J, Watterson M J, Boor K J, Martin N H and Wiedmann M (2015) Spore populations among bulk tank raw milk and dairy powders are significantly different. Journal of Dairy Science 98 8492–8504.
- Milton M E and Cavanagh J (2023) The biofilm regulatory network from Bacillus subtilis: a structure-function analysis. Journal of Molecular Biology 435 167923.
- Msarah M J, Ibrahim I, Hamid A A and Aqma W S (2020) Optimisation and production of alpha amylase from thermophilic Bacillus spp. and its application in food waste biodegradation. Heliyon 6 e04183.
- Navaneethan Y and Effarizah M E (2021) Prevalence, toxigenic profiles, multidrug resistance, and biofilm formation of Bacillus cereus isolated from ready-to eat cooked rice in Penang, Malaysia. Food Control 121 107553.
- Nie L-J, Ye W-Q, Xie W-Y and Zhou W-W (2022) Biofilm: new insights in the biological control of fruits with Bacillus amyloliquefaciens B4. Microbiological Research 265 127196.
- Nwoko E-s Q A and Okeke I N (2021) Bacteria autoaggregation: how and why bacteria stick together. Biochemical Society Transactions 49 1147–1157.
- Ohara H and Yahata M (1996) L-lactic acid production by Bacillus sp. in anaerobic and aerobic culture. Journal of Fermentation and Bioengineering 81 272–274.
- Pan L C, Zhu Y M, Zhu Z Y, Xue W, Liu C Y, Sun H Q and Yue Y (2020) Chemical structure and effects of antioxidation and against α-glucosidase of natural polysaccharide from Glycyrrhiza inflata Batalin. International Journal of Biological Macromolecules 155 560–571.
- Pavithra S, Ramesh R, Aarthy M, Ayyadurai N, Gowthaman M K and Kamini N R (2014) Starchy substrates for production and characterization of Bacillus subtilis amylase and its efficacy in detergent and breadmaking formulations. Starch-Starke 66 976–984.
- Peng P (2024) Yogurt–China–2024. [Internet document] URL https://clients.mintel.com/content/report/suan-nai-zhong-guo-2024nian#workspace_SpacesStore_b4fad3e0-a852-42f3-ac2b-36ca97b58464.
- Prasad S and Purohit S R (2023) Microbial exopolysaccharide: sources, stress conditions, properties and application in food and environment: a comprehensive review. International Journal of Biological Macromolecules 242 124925.
- Rana S and Upadhyay L S B (2020) Microbial exopolysaccharides: synthesis pathways, types and their commercial applications. International Journal of Biological Macromolecules 157 577–583.
- Ringleben L, Weise T, Truong H T T, Anh L H and Pfaff M (2022) Experimental and model-based characterisation of Bacillus spizizenii growth under different temperature, pH and salinity conditions prior to aquacultural wastewater treatment application. Biochemical Engineering Journal 187 108630.
- Ronimus R S, Parker L E, Turner N, Poudel S, Rückert A and Morgan H W (2003) A RAPD-based comparison of thermophilic bacilli from milk powders. International Journal of Food Microbiology 85 45–61.
- Sadiq F A, Li Y, Liu T, Flint S, Zhang G, Yuan L, Pei Z and He G (2016) The heat resistance and spoilage potential of aerobic mesophilic and thermophilic spore forming bacteria isolated from Chinese milk powders. International Journal of Food Microbiology 238 193–201.
- Sandoval-Castilla O, Lobato-Calleros C, Aguirre-Mandujano E and Vernon-Carter E J (2004) Microstructure and texture of yogurt as influenced by fat replacers. International Dairy Journal 14 151–159.
- Sauer K, Stoodley P, Goeres D M, Hall-Stoodley L, Burmolle M, Stewart P S and Bjarnsholt T (2022) The biofilm life cycle: expanding the conceptual model of biofilm formation. Nature Reviews Microbiology 20 608–620.
- Staffolo M D, Bertola N, Martino M and Bevilacqua A (2004) Influence of dietary fiber addition on sensory and rheological properties of yogurt. International Dairy Journal 14 263–268.
- Tabilo-Munizaga G and Barbosa-Cánovas G V (2005) Rheology for the food industry. Journal of Food Engineering 67 147–156.
- Tantray J A, Mansoor S, Wani R F C and Nissa N U (2023) Chapter 17 – Estimation of reducing sugar by using dinitro salicylic acid method. In Basic Life Science Methods, pp. 69–73. J A Tantray, S Mansoor, R F C Wani and N U Nissa, eds. Cambridge, MA: Academic Press.
10.1016/B978-0-443-19174-9.00017-9 Google Scholar
- Tian H, Li B L, Evivie S E, Sarker S K, Chowdhury S, Lu J J, Ding X Y and Huo G C (2018) Technological and genomic analysis of roles of the cell-envelope protease PrtS in yoghurt starter development. International Journal of Molecular Sciences 19 1068.
- Trunet C, Carlin F and Coroller L (2017) Investigating germination and outgrowth of bacterial spores at several scales. Trends in Food Science & Technology 64 60–68.
- Trunk T, Khalil H S and Leo J C (2018) Bacterial autoaggregation. AIMS Microbiology 4 140–164.
- Valero M, Fernández P S and Salmerón M C (2003) Influence of pH and temperature on growth of Bacillus cereus in vegetable substrates. International Journal of Food Microbiology 82 71–79.
- Vandana Priyadarshanee M and Das S (2023) Bacterial extracellular polymeric substances: biosynthesis and interaction with environmental pollutants. Chemosphere 332 138876.
- Vuotto C, Longo F, Pascolini C, Donelli G, Balice M P, Libori M F, Tiracchia V, Salvia A and Varaldo P E (2017) Biofilm formation and antibiotic resistance in Klebsiella pneumoniae urinary strains. Journal of Applied Microbiology 123 1003–1018.
- Wang N, Sadiq F A, Li S, He G and Yuan L (2020) Tandem mass tag-based quantitative proteomics reveals the regulators in biofilm formation and biofilm control of Bacillus licheniformis. Food Control 110 107029.
- Wang N, Gao J, Yuan L, Jin Y and He G (2021) Metabolomics profiling during biofilm development of Bacillus licheniformis isolated from milk powder. International Journal of Food Microbiology 337 108939.
- Wang N, Jin Y, He G and Yuan L (2022) Dynamic tracing of bacterial community distribution and biofilm control of dominant species in milk powder processing. LWT 154 112855.
- Xavier A R E O, Lima E R, Oliveira A M E et al. (2017) Genetic diversity of Bacillus sp producers of amylase isolated from the soil. Genetics and Molecular Research 16 1–10.
- Yan Z, Zheng X W, Chen J Y, Han J S and Han B Z (2013) Effect of different Bacillus strains on the profile of organic acids in a liquid culture of Daqu. Journal of the Institute of Brewing 119 78–83.
- Yang X, Wang Z, Zhang C, Wang L, Pang L, Zhang D, Man C and Jiang Y (2021) Assessment of the production of Bacillus cereus protease and its effect on the quality of ultra-high temperature-sterilized whole milk. Journal of Dairy Science 104 6577–6587.
- Yuan D-D, Liu G-C, Ren D-Y, Zhang D, Zhao L, Kan C P, Yang Y Z, Ma W, Li Y and Zhang L B (2012) A survey on occurrence of thermophilic bacilli in commercial milk powders in China. Food Control 25 752–757.
- Zhao X, Chen G, Wang F, Zhao H, Wei Y, Liu L and Zhang H (2022) Extraction, characterization, antioxidant activity and rheological behavior of a polysaccharide produced by the extremely salt tolerant Bacillus subtilis LR-1. LWT 162 113413.