Abstract
This study aimed to isolate lactic acid bacteria (LABs) of technological interest from Moroccan camel milk and select starter or adjunct culture for dairy product manufacturing. The phenotypic and biochemical identification of 47 isolates revealed the existence of ten Lactococcus lactis, eleven Lactobacillus plantarum, three Lactobacillus brevis, two Lactobacillus paracasei, eleven Enterococcus spp., seven Lactococcus spp. and two Lactobacillus spp. Our strains showed a fast acidifying ability (ΔpH ranged between 0.69 ± 0.01 and 1.22 ± 0.05 after 6 h), high proteolytic and autolytic activities (1.93 ± 0.02 to 9.9 ± 0.022 mM glycine and 15.21 ± 2.21% to 83.24 ± 1% respectively), and an important lipolytic and free radical scavenging capacity. Furthermore, they were able to use citrate, to produce exopolysaccharide, and they exhibited antibacterial activity against Gram-negative and Gram-positive pathogenic bacteria and had no hemolytic activity. This study has shown that Moroccan camel milk represents a rich biotope of interesting LABs for dairy products industry.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Abera T, Legesse Y, Mummed B, Urga B (2016) Bacteriological quality of raw camel milk along the market value chain in Fafen zone, Ethiopian Somali regional state. BMC Res Notes 9(285):1–6. https://doi.org/10.1186/s13104-016-2088-1
Abushelaibi A, Al-Mahadin S, El-Tarabily K, Shah NP, Ayyash M (2017) Characterization of potential probiotic lactic acid bacteria isolated from camel milk. LWT-Food Sci Technol 79:316–325. https://doi.org/10.1016/j.lwt.2017.01.041
Akabanda F, Owusu-Kwarteng J, Tano-Debrah K, Parkouda C, Jespersen L (2014) The use of lactic acid bacteria starter culture in the production of Nunu, a spontaneously fermented milk mroduct in Ghana. Int J Food Sci 2014:1–11. https://doi.org/10.1155/2014/721067
Akhmetsadykova SH, Baubekova A, Konuspayeva G, Akhmetsadykova N, Faye B, Loiseau G (2015) Lactic acid bacteria biodiversity in raw and fermented camel milk. Afr J Food Sci Technol 6:84–88. https://doi.org/10.14303/ajfst.2015.026
Al haj OA, Al Kanhal HA, (2010) Compositional, technological and nutritional aspects of dromedary camel milk. Int Dairy J 20:811–821. https://doi.org/10.1016/j.idairyj.2010.04.003
Alaoui Ismaili M, Saidi B, Zahar M, Hamama A, Ezzaier R (2016) Composition and microbial quality of raw camel milk produced in Morocco. J Saudi Soc Agric Sci 18:17–21. https://doi.org/10.1016/j.jssas.2016.12.001
Aluko RE (2012) Functional foods and nutraceuticals. Springer, New York, NY
Aly SA, Elewa N (2014) Hazards associated with dromedary camel milks. Int j Sci Nat 5:412–417
AOAC (2000) Official methods of analysis. (17th ed.). Association of official Analytical Chemists
Ayyash M, Abushelaibi A, Al-Mahadin S, Enan M, El-Tarabily K, Shah N (2018) In-vitro investigation into probiotic characterisation of Streptococcus and Enterococcus isolated from camel milk. Lwt-Food Sci Technol 87:478–487. https://doi.org/10.1016/j.lwt.2017.09.019
Ayyash M, Al-Nuaimi AK, Al-Mahadin S, Liu SQ (2017) In vitro investigation of anticancer and ACE-inhibiting activity. α-amylase and α-glucosidase inhibition and antioxidant activity of camel milk fermented with camel milk probiotic: a comparative study with fermented bovine milk. Food Chem 239:588–597. https://doi.org/10.1016/j.foodchem.2017.06.149
Badis A, Guetarni D, Moussa-Boudjemâa B, Henni DE, Tornadijo ME, Kihal M (2004) Identification of cultivable lactic acid bacteria isolated from Algerian raw goat’s milk and evaluation of their technological properties. Food Microbiol 21:343–349. https://doi.org/10.1016/s0740-0020(03)00072-8
Bekele B, Hansen EB, Eshetu M, Ipsen R, Hailu Y (2018) Effect of starter cultures on properties of soft white cheese made from camel (Camelus dromedarius) milk. J Dairy Sci 102:1–8. https://doi.org/10.3168/jds.2018-15084
Belkheir K , Centeno JA, Zadi-Karam H, Karam NE, Carballo J (2016) Potential technological interest of indigenous lactic acid bacteria from algerian camel milk Ital J Food Sci 28:598-611
Benkerroum N, Boughdadi A, Bennani N, Hidane K (2003) Microbiological quality assessment of Moroccan camel’s milk and identification of predominating lactic acid bacteria. World J Microbiol Biotechnol 19:645–648. https://doi.org/10.1023/A:1025114601811
Beresford TP (2011) Lactic acid bacteria : citrate fermentation by lactic acid bacteria Encyclopedia of Dairy Sciences 166–172 https://doi.org/10.1016/b978-0-12-374407-4.00272-7
Bonomo MG, Salzano G (2013) Genotypic and technological diversity of Leuconostoc mesenteroides and Lactobacillus paracasei ssp. paracasei strains for use as adjunct starter cultures in Pecorino di Filiano cheese. Int J Dairy Technol 66:402–409. https://doi.org/10.1111/1471-0307.12040
Bourdat-Deschamps M, Le Bars D, Yvon M, Chapot-Chartier MP (2004) Autolysis of Lactococcus lactis AM2 stimulates the formation of certain aroma compounds from amino acids in a cheese model. Int Dairy J 14:791–800. https://doi.org/10.1016/j.idairyj.2004.02.009
Carafa I, Nardin T, Larcher R, Viola R, Tuohy K, Franciosi E (2015) Identification and characterization of wild lactobacilli and pediococci from spontaneously fermented mountain cheese. Food Microbiol 48:123–132. https://doi.org/10.1016/j.fm.2014.12.003
Comasio A, Harth H, Weckx S, De Vuyst L (2019) The addition of citrate stimulates the production of acetoin and diacetyl by a citrate-positive Lactobacillus crustorum strain during wheat sourdough fermentation. Int J Food Microbiol 289:88–105. https://doi.org/10.1016/j.ijfoodmicro.2018.08.030
Domingos-Lopes MFP, Stanton C, Ross PR, Dapkevicius MLE, Silva CCG (2017) Genetic diversity, safety and technological characterization of lactic acid bacteria isolated from artisanal Pico cheese. Food Microbiol 63:178–190. https://doi.org/10.1016/j.fm.2016.11.014
Edalati E, Saneei B, Alizadeh M, Hosseini SS, bialvaei AZ, Taheri K, (2018) Isolation of probiotic bacteria from raw camel milk and their antagonistic effects on two bacteria causing food poisoning. New Microbes New Infect 27:64–68. https://doi.org/10.1016/j.nmni.2018.11.008
El Hatmi H, Jrad Z, Oussaief O, Nasri W, Sbissi I, Khorchani T, Canabady-Rochelle LLS (2018) Fermentation of dromedary camel (Camelus dromedarius ) milk by Enterococcus faecium, Streptococcus macedonicus as a potential alternative of fermented cow milk. LWT - Food Sci Technol 90:373–380. https://doi.org/10.1016/j.lwt.2017.12.040
Elagamy E (2006) Camel milk. In :Y.W. Park et G. F. Haenlein (Eds) Handbook of Milk of Non bovine Mammals, 1st edition. USA: Blackwell Publishing Professional, pp 297–344
Elfahri KR, Donkor ON, Vasiljevic T (2014) Potential of novel Lactobacillus helveticus strains and their cell wall bound proteases to release physiologically active peptides from milk proteins. Int Dairy J 38:37–46. https://doi.org/10.1016/j.idairyj.2014.03.010
Foulquié Moreno MR, Sarantinopoulos P, Tsakalidou E, De Vuyst L (2006) The role and application of Enterococci in food and health. Int J Food Microbiol 106:1–24. https://doi.org/10.1016/j.ijfoodmicro.2005.06.026
Gänzle MG (2015) Lactic metabolism revisited: metabolism of lactic acid bacteria in food fermentations and food spoilage. Curr Opin Food Sci 2:106–117. https://doi.org/10.1016/j.cofs.2015.03.001
García-Cano I, Rocha-Mendoza D, Ortega-Anaya J, Wang K, Kosmerl E, Jiménez-Flores R (2019) Lactic acid bacteria isolated from dairy products as potential producers of lipolytic, proteolytic and antibacterial proteins. Appl Microbiol Biotechnol 103:5243–5257. https://doi.org/10.1007/s00253-019-09844-6
Gatti M, Bottari B, Lazzi C, Neviani E, Mucchetti G (2014) Invited review: microbial evolution in raw milk, long-ripened cheeses produced using undefined natural whey starters. J Dairy Sci 97:573–591. https://doi.org/10.3168/jds.2013-7187
Ginalska G, Bancerz R, Korniłłowicz-Kowalska T (2004) A thermostable lipase produced by a newly isolated Geotrichum-like strain R59. J Ind Microbiol Biotechnol 31:177–182. https://doi.org/10.1007/s10295-004-0134-9
Graham K, Rea R, Simpson P, Stack H (2017) Development of a rapid, one-step screening method for the isolation of presumptive proteolytic enterococci. J Microbiol Methods 132:99–105. https://doi.org/10.1016/j.mimet.2016.11.016
Hassaïne O, Zadi-Karam H, Karam NE (2007) Technologically important properties of lactic acid bacteria isolated from raw milk of three breeds of Algerian dromedary (Camelus dromedarius). Afr J Biotechnol 6:1720–1727. https://doi.org/10.5897/AJB2007.000-2251
Iranmanesh M, Ezzatpanah H, Mojgani N (2014) Antibacterial activity and cholesterol assimilation of lactic acid bacteria isolated from traditional Iranian dairy products. LWT - Food Sci Technol 58:355–359. https://doi.org/10.1016/j.lwt.2013.10.005
Izadi A, Khedmat L, Mojtahedi SY (2019) Nutritional and therapeutic perspectives of camel milk and its protein hydrolysates: a review on versatile biofunctional properties. J Funct Foods 60(103441):1–13. https://doi.org/10.1016/j.jff.2019.103441
Kadri Z, Spitaels F, Cnockaert M, Amar M, Joossens M, Vandamme P (2021) The bacterial diversity of raw Moroccon camel milk Int J Food Microbiol 341:109050:1-8https://doi.org/10.1016/j.ijfoodmicro.2021.109050
Kempler GM, Mc Kay LL (1980) Improved medium for detection of citrate-fermenting Streptococcus lactis subsp. diacetylactis. Appl Environ Microbiol 39:926–927
Khalesi M, Salami M, Moslehishad M, Winterburn J, Moosavi-Movahedi AA (2017) Biomolecular content of camel milk: a traditional superfood towards future healthcare industry. Trends Food Sci Technol 62:49–58. https://doi.org/10.1016/j.tifs.2017.02.004
Khan IT, Nadeem M, Imran M, Ullah R, Ajmal M, Jaspal MH (2019) Antioxidant properties of Milk and dairy products: a comprehensive review of the current knowledge. Lipids Health Dis 18(41):1–13. https://doi.org/10.1186/s12944-019-0969-8
Khedid K, Faid M, Mokhtari A, Soulaymani A, Zinedine A (2009) Characterization of lactic acid bacteria isolated from the one humped camel milk produced in Morocco. Microbiol Res 164:81–91. https://doi.org/10.1016/j.micres.2006.10.008
Konuspayeva G, Faye B, Loiseau G (2009) The composition of camel milk: a meta analysis of the literature data. J Food Compos Anal 22:95–101
Mahmoudi I, Moussa OB, Khaldi TEM, Kebouchi M, Soligot C, Le Roux Y, Hassouna M (2016) Functional in vitro screening of Lactobacillus strains isolated from Tunisian camel raw milk toward their selection as probiotic. Small Rumin Res 137:91–98. https://doi.org/10.1016/j.smallrumres.2016.03.016
Marroki A, Bousmaha-Marroki L (2014) Lactobacilli isolated from Algerian goat’s milk as adjunct culture in dairy products. Braz Arch Biol Technol 57:410–420. https://doi.org/10.1590/S1516-89132014005000003
Meng Z, Zhang L, Xin L, Lin K, Yi H, Han X (2018) Technological characterization of Lactobacillus in semihard artisanal goat cheeses from different Mediterranean areas for potential use as nonstarter lactic acid bacteria. Int J Dairy Sci 101:2887–2896. https://doi.org/10.3168/jds.2017-14003
Mora D, Musacchio F, Senini FMG, L, Manachini PL (2003) Autolytic activity and pediocin-induced lysis in Pediococcus acidilactici and Pediococcus pentosaceus strains. J Appl Microbiol 94:561–570. https://doi.org/10.1046/j.1365-2672.2003.01868.x
Moslehishad M, Mirdamadi S, Ehsani MR, Ezzatpanah H, Moosavi-Movahedi AA (2013) The proteolytic activity of selected lactic acid bacteria in fermenting cow’s and camel’s milk and the resultant sensory characteristics of the products. Int J Dairy Technol 66:279–285. https://doi.org/10.1111/1471-0307.12017
Nieto-Arribas P, Sesena S, Poveda GM, Palop L (2010) Genotypic and technological characterization of Leuconostoc isolates to be used as adjunct starters in Manchego cheese manufacture. Food Microbiol 27:85–93. https://doi.org/10.1016/j.fm.2009.08.006
Orf K, Cunnington AJ (2015) Infection-related hemolysis and susceptibility to Gram-negative bacterial co-infection. Front Microbiol 6(666):1–8. https://doi.org/10.3389/fmicb.2015.00666
Ouattara HD, Ouattara HG, Droux M, Reverchon S, Nasser W, Niamke SL (2017) Lactic acid bacteria involved in cocoa beans fermentation from Ivory Coast: species diversity and citrate lyase production. Int J Food Microbiol 256:11–19. https://doi.org/10.1016/j.ijfoodmicro.2017.05.008
Perin LM, Miranda RO, Todorov SD, de Franco BDG, M, Nero LA, (2014) Virulence, antibiotic resistance and biogenic amines of bacteriocinogenic lactococci and enterococci isolated from goat milk. Int J Food Microbiol 185:121–126. https://doi.org/10.1016/j.ijfoodmicro.2014.06.001
Rahbar Saadat Y, Yari Khosroushahi A, Pourghassem Gargari B (2019) A comprehensive review of anticancer, immunomodulatory and health beneficial effects of the lactic acid bacteria exopolysaccharides. Carbohydr Polym 217:79–89. https://doi.org/10.1016/j.carbpol.2019.04.025
Rahmeh R, Akbar A, Kishk M, Al-Onaizi T, Al-Azmi A, Al-Shatti A, Shajan A, Al-Mutairi S, Akbar B (2019) Distribution and antimicrobial activity of lactic acid bacteria from raw camel milk. New Microbes New Infect 30(100560):1–8. https://doi.org/10.1016/j.nmni.2019.100560
Ramírez-Nuñez J, Romero-Medrano R, Nevárez-Moorillón GV, Gutiérrez-Méndez N (2011) Effect of pH and salt gradient on the autolysis of Lactococcus lactis strains. Braz J Microbiol 42:1495–1499. https://doi.org/10.1590/s1517-83822011000400036
Shokri H, Torabi S (2016) The effect of milk composition: yeast-mould numbers and seasons on aflatoxin M1 amounts in camel milk. J Food Saf 37:421–425. https://doi.org/10.1111/jfs.12300
Silva CCG, Silva SPM, Ribeiro SC (2018) Application of bacteriocins and protective cultures in dairy food preservation. Front Microbiol 9:594–609. https://doi.org/10.3389/fmicb.2018.00594
Silva EOO, Nespolo CR, Sehn C, Pinheiro FC, Stefani LM (2019) Lactic acid bacteria with antimicrobial, proteolytic and lipolytic activities isolated from ovine dairy products. Food Sci Technol 40:293–299. https://doi.org/10.1590/fst.11019
Soleymanzadeh N, Mirdamadi S, Kianirad M (2016) Antioxidant activity of camel and bovine milk fermented by lactic acid bacteria isolated from traditional fermented camel milk (Chal). Dairy Sci Technol 96:443–457. https://doi.org/10.1007/s13594-016-0278-1
Suzuki-Iwashima A, Matsuura H, Iwasawa A, Shiota M (2019) Metabolomics analyses of the combined effects of lactic acid bacteria and Penicillium camemberti on the generation of volatile compounds in model mold-surface-ripened cheeses. J Biosci Bioeng 129:333–347. https://doi.org/10.1016/j.jbiosc.2019.09.005
Tagliazucchi D, Martini S, Solieri L (2019) Bioprospecting for bioactive peptide production by lactic acid bacteria isolated from fermented dairy food. Fermentation 5:96–130. https://doi.org/10.3390/fermentation5040096
Viana de Souza J, Silva Dias F (2017) Protective, technological and functional properties of select autochthonous lactic acid bacteria from goat dairy products. Curr Opin Food Sci 13:1–9. https://doi.org/10.1016/j.cofs.2017.01.003
Virtanen T, Pihlanto A, Akkanen S, Korhonen H (2007) Development of antioxidant activity in milk whey during fermentation with lactic acid bacteria. J Appl Microbiol 102:106–115. https://doi.org/10.1111/j.1365-
Widyastuti Y, Rohmatussolihat R, Febrisiantosa A (2014) The role of lactic acid bacteria in milk fermentation. Food Nutr Sci 5:435–442. https://doi.org/10.4236/fns.2014.54051
Younan M (2004) Milk hygiene and udder health. In: Farah Z. Fischer A. editors.Milk and meat from the camel-Handbook on products and processing. vdf Hochschulverlag AG. ETH Zuerich. Zuerich/Singen. Switzerland; 2004
Zaaraoui L, Ounine K, El Hamdani M, Benali A, Oukassou M, Bouksaim M (2016) Evaluation and selection of autochthonous lactic acid bacteria as starter cultures from goat’s raw milk. J Biotechnol Biochem 2:16–21
Zhao J, Fan H, Kwok LY, Guo F, Ji R, Ya M, Chen Y (2019) Analyses of physicochemical properties, bacterial microbiota, and lactic acid bacteria of fresh camel milk collected in Inner Mongolia. J Dairy Sci 103:106–116. https://doi.org/10.3168/jds.2019-17023
Acknowledgements
The authors thank Mr. Amine Rkhaila from the laboratory of Plant, Animal, and Agro-industry Productions, Ibn Tofail University, Faculty of Sciences, for his revision of the form and grammar of the manuscript.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no competing interests.
Additional information
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
Moussaid, S., Bouhlal, O., Benali, A. et al. Technological characterization of indigenous lactic acid bacteria from Moroccan camel milk for their potential use as starter or adjunct culture. Folia Microbiol 66, 761–774 (2021). https://doi.org/10.1007/s12223-021-00885-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12223-021-00885-x