Draft Genome Sequence of Lactococcus lactis Subsp. cremoris WA2-67: A Promising Nisin-Producing Probiotic Strain Isolated from the Rearing Environment of a Spanish Rainbow Trout (Oncorhynchus mykiss, Walbaum) Farm
Abstract
:1. Introduction
2. Materials and Methods
2.1. Growth Conditions and Genomic DNA Isolation
2.2. Draft Genome Sequencing, Assembly, and Map**
2.3. Bioinformatic In Silico Analysis
2.3.1. Identification
2.3.2. Probiotic Traits
2.3.3. Bacteriocin Production
2.3.4. Mobile Genetic Elements (MGE)
Insertion Sequences (IS)
Plasmids
Prophages
2.3.5. CRISPR/CRISPR-Cas
2.3.6. Transferable Antibiotic Resistances
2.3.7. Virulence Factors
3. Results and Discussion
3.1. Draft Genome Sequencing, Assembly, and Map**
3.2. Bioinformatic In Silico Analysis
3.2.1. Identification
3.2.2. Probiotic Traits
3.2.3. Bacteriocin Production
3.2.4. MGE (IS, Plasmids and Prophages)
3.2.5. CRISPR/CRISPR-Cas
3.2.6. Transferable Antibiotic Resistances
3.2.7. Virulence Factors
4. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Defoirdt, T.; Sorgeloos, P.; Bossier, P. Alternatives to antibiotics for the control of bacterial disease in aquaculture. Curr. Opin. Microbiol. 2011, 14, 251–258. [Google Scholar] [CrossRef]
- FAO. The State of World Fisheries and Aquaculture; FAO Fisheries and Aquaculture Department: Rome, Italy, 2020. [Google Scholar]
- Infante-Villamil, S.; Huerlimann, R.; Jerry, D.R. Microbiome diversity and dysbiosis in aquaculture. Rev. Aquac. 2021, 13, 1077–1096. [Google Scholar] [CrossRef]
- United Nations. World Population Prospects: The 2017 Revision, Key Findings and Advance Tables; Population Division, Working Paper No. ESA/P/WP/248; Department of Economic and Social Affairs: New York, NY, USA, 2017. [Google Scholar]
- Cabello, F.C.; Godfrey, H.P.; Buschmann, A.H.; Dölz, H.J. Aquaculture as yet another environmental gateway to the development and globalisation of antimicrobial resistance. Lancet Infect. Dis. 2016, 16, e127–e133. [Google Scholar] [CrossRef]
- Zhao, Y.; Yang, Q.E.; Zhou, X.; Wang, F.; Muurinen, J.; Virta, M.P.; Brandt, K.K.; Zhu, Y. Antibiotic resistome in the livestock and aquaculture industries: Status and solutions. Crit. Rev. Environ. Sci. 2021, 51, 2159–2196. [Google Scholar] [CrossRef]
- Pérez-Sánchez, T.; Ruiz-Zarzuela, I.; de Blas, I.; Balcázar, J.L. Probiotics in aquaculture: A current assessment. Rev. Aquac. 2014, 6, 133–146. [Google Scholar] [CrossRef]
- Gómez-Sala, B.; Feito, J.; Hernández, P.E.; Cintas, L.M. Lactic Acid Bacteria in aquatic environments and their applications. In Lactic Acid Bacteria: Microbiological and Functional Aspects, 5th ed.; Vinderola, G., Ouwehand, A.C., Salminen, S., von Wright, A., Eds.; CRC Press: Boca Raton, FL, USA, 2019; pp. 555–570. [Google Scholar]
- Wu, X.; Teame, T.; Hao, Q.; Ding, Q.; Liu, H.; Ran, C.; Yang, Y.; Zhang, Y.; Zhou, Z.; Duan, M.; et al. Use of a paraprobiotic and postbiotic feed supplement (HWF™) improves the growth performance, composition and function of gut microbiota in hybrid sturgeon (Acipenser baerii × Acipenser schrenckii). Fish Shellfish Immunol. 2020, 104, 36–45. [Google Scholar] [CrossRef]
- Rychen, G.; Aquilina, G.; Azimonti, G.; Bampidis, V.; Bastos, M.L.; Bories, G.; Chesson, A.; Cocconcelli, P.S.; Flachowsky, G.; Gropp, J.; et al. Guidance on the characterization of microorganisms used as feed additives or as production organisms. EFSA J. 2018, 16, e05206. [Google Scholar] [PubMed]
- EFSA (European Food Safety Authority). EFSA statement on the requirements for whole genome sequence analysis of microorganisms intentionally used in the food chain. EFSA J. 2021, 19, e06506. [Google Scholar]
- Fečkaninová, A.; Koščová, J.; Mudroňová, D.; Popelka, P.; Toropilová, J. The use of probiotic bacteria against Aeromonas infection in salmonid aquaculture. Aquaculture 2017, 469, 1–8. [Google Scholar] [CrossRef]
- Cintas, L.M.; Herranz, C.; Hernández, P.E. Natural and heterologous production of bacteriocins. In Prokaryotic Antimicrobial Peptides: From Genes to Applications, 1st ed.; Drider, D., Rebufatt, S., Eds.; Springer: Dordrecht, The Netherlands, 2011; pp. 115–143. [Google Scholar]
- Araújo, C.; Muñoz-Atienza, E.; Nahuelquín, Y.; Poeta, P.; Igrejas, G.; Hernández, P.E.; Herranz, C.; Cintas, L.M. Inhibition of fish pathogens by the microbiota from rainbow trout (Oncorhynchus mykiss, Walbaum) and rearing environment. Anaerobe 2015, 32, 7–14. [Google Scholar] [CrossRef]
- Araújo, C.; Muñoz-Atienza, E.; Ramírez, M.; Poeta, P.; Igrejas, G.; Hernández, P.E.; Herranz, C.; Cintas, L.M. Safety assessment, genetic relatedness and bacteriocin activity of potential probiotic Lactococcus lactis strains from rainbow trout (Oncorhynchus mykiss, Walbaum) and rearing environment. Eur. Food Res. Technol. 2015, 241, 647–662. [Google Scholar] [CrossRef]
- Araújo, C.; Muñoz-Atienza, E.; Pérez-Sánchez, T.; Poeta, P.; Igrejas, G.; Hernández, P.E.; Herranz, C.; Ruiz-Zarzuela, I.; Cintas, L.M. Nisin Z production by Lactococcus lactis subsp. cremoris WA2-67 of aquatic origin as a defense mechanism to protect rainbow trout (Oncorhynchus mykiss, Walbaum) against Lactococcus garvieae. Mar. Biotechnol. 2015, 17, 820–830. [Google Scholar] [CrossRef] [PubMed]
- Velásquez, J.E.; van der Donk, W. Genome mining for ribosomally synthesized natural products. Curr. Opin. Chem. Biol. 2011, 15, 11–21. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kapse, N.G.; Engineer, A.S.; Gowdaman, V.; Wagh, S.; Dhakephalkar, P.K. Functional annotation of the genome unravels probiotic potential of Bacillus coagulans HS243. Genomics 2019, 111, 921–929. [Google Scholar] [CrossRef]
- Hussein, W.E.; Abdelhamid, A.G.; Rocha-Mendoza, D.; Garcia-Cano, I.; Yousef, A.E. Assessment of safety and probiotic traits of Enterococcus durans OSY-EGY, isolated from Egyptian artisanal cheese, using comparative genomics and phenotypic analysis. Front. Microbiol. 2020, 11, 3094. [Google Scholar] [CrossRef]
- ** of plasmids using PlasmidFinder and plasmid multilocus sequence ty**. Antimicrob. Agents Chemother. 2014, 58, 3895–3903. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Camacho, C.; Coulouris, G.; Avagyan, V.; Ma, N.; Papadopoulos, J.; Bealer, K.; Madden, T.L. BLAST+: Architecture and applications. BMC Bioinform. 2009, 10, 421. [Google Scholar] [CrossRef] [Green Version]
- Song, W.; Sun, H.; Zhang, C.; Cheng, L.; Peng, Y.; Deng, Z.; Wang, D.; Wang, Y.; Hu, M.; Liu, W.; et al. Prophage Hunter: An integrative hunting tool for active prophages. Nucleic Acids Res. 2019, 47, W74–W80. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Couvin, D.; Bernheim, A.; Toffano-Nioche, C.; Touchon, M.; Michalik, J.; Néron, B.; Rocha, E.; Vergnaud, G.; Gautheret, D.; Pourcel, C. CRISPRCasFinder, an update of CRISRFinder, includes a portable version, enhanced performance and integrates search for Cas proteins. Nucleic Acids Res. 2018, 46, W246–W251. [Google Scholar] [CrossRef] [Green Version]
- Bortolaia, V.; Kaas, R.F.; Ruppe, E.; Roberts, M.C.; Scharwz, S.; Cattoir, V.; Philippon, A.; Allesoe, R.L.; Rebelo, A.R.; Florensa, A.R.; et al. ResFinder 4.0 for predictions of phenotypes from genotypes. J. Antimicrob. Chemother. 2020, 75, 3491–3500. [Google Scholar] [CrossRef] [PubMed]
- Joensen, K.G.; Scheutz, F.; Lund, O.; Hasman, H.; Kaas, R.S.; Nielsen, E.M.; Aarestrup, F.M. Real-time whole-genome sequencing for routine ty**, surveillance, and outbreak detection of verotoxigenic Escherichia coli. J. Clin. Microbiol. 2014, 52, 1501–1510. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Cosentino, S.; Larsen, M.V.; Aarestrup, F.M.; Lund, O. PathogenFinder—Distinguishing friend from foe using bacterial Whole Genome Sequence data. PLoS ONE 2013, 8, e77302. [Google Scholar] [CrossRef]
- Kapse, N.G.; Engineer, A.S.; Gowdaman, V.; Wagh, S.; Dhakephalkar, P.K. Genome profiling for health promoting and disease preventing traits unraveled probiotic potential of Bacillus clausii B106. Microbiol. Biotechnol. Lett. 2018, 46, 334–345. [Google Scholar] [CrossRef]
- Wang, W.; Sun, J.; Liu, C.; Xue, Z. Application of immunostimulants in aquaculture: Current knowledge and future perspectives. Aquac. Res. 2017, 48, 1–23. [Google Scholar] [CrossRef]
- Wang, C.; Chuprom, J.; Wang, Y.; Fu, L. Beneficial bacteria for aquaculture: Nutrition, bacteriostasis and immunoregulation. J. Appl. Microbiol. 2020, 128, 28–40. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ghosh, S.; Sinha, A.; Sahu, C. Effect of probiotic on reproductive performance in female livebearing ornamental fish. Aquac. Res. 2007, 38, 518–526. [Google Scholar] [CrossRef]
- Honeyfield, D.C.; Hinterkopf, J.P.; Fitzsimons, J.D.; Zajicek, J.L.; Brown, S.B. Development of thiamine deficiencies and Early Mortality Syndrome in lake trout by feeding experimental and feral fish diets containing thiaminase. J. Aquac. Anim. Health 2005, 17, 4–12. [Google Scholar] [CrossRef]
- Yossa, R.; Sarker, P.K.; Mock, D.M.; Lall, S.P. Vanderberg, G.W. Current knowledge on biotin nutrition in fish and research perspectives. Rev. Aquac. 2015, 7, 59–73. [Google Scholar] [CrossRef]
- Maeland, A.; Rønnestad, I.; Waagbø, R. Folate in eggs and develo** larvae of Atlantic halibut, Hippoglossus hippoglossus, L. Aquac. Nutr. 2003, 9, 185–188. [Google Scholar] [CrossRef]
- Oliva-Teles, A. Nutrition and health of aquaculture fish. J. Fish Dis. 2012, 35, 83–108. [Google Scholar] [CrossRef] [PubMed]
- Hoseini, S.M.; Khan, M.A.; Yousefi, M.; Costas, B. Roles of arginine in fish nutrition and health: Insights for future research. Rev. Aquac. 2020, 12, 2091–2108. [Google Scholar] [CrossRef]
- Hoseini, S.M.; Pérez-Jiménez, A.; Costas, B.; Azeredo, R.; Gesto, M. Physiological roles of tryptophan in teleosts: Current knowledge and perspectives for future studies. Rev. Aquac. 2019, 11, 3–24. [Google Scholar] [CrossRef] [Green Version]
- Sarih, S.; Djellata, A.; Roo, J.; Hernández-Cruz, C.M.; Fontanillas, R.; Rosenlund, G.; Izquierdo, M.; Fernández-Palacios, H. Effects of increased protein, histidine and taurine dietary levels on egg quality of greater amberjack (Seriola dumerili, Risso, 1810). Aquaculture 2019, 499, 72–79. [Google Scholar] [CrossRef]
- Zhang, H.; HuangFu, H.; Wang, X.; Zhao, S.; Liu, Y.; Lv, H.; Qin, G.; Tan, Z. Antibacterial activity of lactic acid producing Leuconostoc mesenteroides QZ1178 against pathogenic Gallibacterium anatis. Front. Vet. Sci. 2021, 8, 630294. [Google Scholar] [CrossRef]
- Pessione, E. Lactic acid bacteria contribution to gut microbiota complexity: Lights and shadows. Front. Cell. Infect. Microbiol. 2012, 2, 86. [Google Scholar] [CrossRef] [Green Version]
- Chang, D.; Jung, H.; Rhee, J.; Pan, J. Homofermentative production of D- or L-lactate in metabolically engineered Escherichia coli RR1. Appl. Environ. Microbiol. 1999, 65, 1384–1389. [Google Scholar] [CrossRef] [Green Version]
- Lorenz, I. D-lactic acidosis in calves. Vet. J. 2009, 179, 197–203. [Google Scholar] [CrossRef]
- Wouters, J.A.; Frenkiel, H.; de Vos, W.M.; Kuipers, O.P.; Abee, T. Cold shock proteins of Lactococcus lactis MG1363 are involved in cryoprotection and in the production of cold-induced proteins. Appl. Environ. Microbiol. 2001, 67, 5171–5178. [Google Scholar] [CrossRef] [Green Version]
- Zhou, Z.; Tang, H.; Wang, W.; Zhang, L.; Su, F.; Wu, Y.; Bai, L.; Li, S.; Sun, Y.; Tao, F.; et al. A cold shock protein promotes high-temperature microbial growth through binding to diverse RNA species. Cell Discov. 2021, 7, 15. [Google Scholar] [CrossRef]
- Ding, W.K.; Shah, N.P. Acid, bile, and heat tolerance of free and microencapsulated probiotic bacteria. J. Food Sci. 2007, 72, M446–M450. [Google Scholar] [CrossRef] [PubMed]
- Nag, A.; Das, S. Improving ambient temperature stability of probiotics with stress adaptation and fluidized bed drying. J. Funct. Foods. 2013, 5, 170–177. [Google Scholar] [CrossRef]
- Domínguez-Maqueda, M.; Cerezo, I.M.; Tapia-Paniagua, S.T.; de la Banda, I.G.; Moreno-Ventas, X.; Moriñigo, M.Á.; Balebona, M.C. A tentative study of the effects of heat-inactivation of the probiotic strain Shewanella putrefaciens Ppd11 on Senegalese sole (Solea senegalensis) intestinal microbiota and immune response. Microorganisms 2021, 9, 808. [Google Scholar] [CrossRef] [PubMed]
- Ventura, M.; Canchaya, C.; Zink, R.; Fitzgerald, G.F.; van Sinderen, D. Characterization of the groEL and groES loci in Bifidobacterium breve UCC 2003: Genetic, transcriptional, and phylogenetic analyses. Appl. Environ. Microbiol. 2004, 70, 6197–6209. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Duru, I.C.; Ylinen, A.; Belanov, S.; Pulido, A.A.; Paulin, L.; Auvinen, P. Transcriptomic time-series analysis of cold- and heat-shock response in psychrotrophic lactic acid bacteria. BMC Genom. 2021, 22, 28. [Google Scholar] [CrossRef]
- Naylor, R.L.; Hardy, R.W.; Buschmann, A.H.; Bush, S.R.; Cao, L.; Klinger, D.H.; Little, D.C.; Lubchenco, J.; Shumway, S.E.; Troell, M. A 20-year retrospective review of global aquaculture. Nature 2021, 591, 551–563. [Google Scholar] [CrossRef]
- Maas, R.M.; Verdegem, M.C.J.; Stevens, T.L.; Schrama, J.W. Effect of exogenous enzymes (phytase and xylanase) supplementation on nutrient digestibility and growth performance of Nile tilapia (Oreochromis niloticus) fed different quality diets. Aquaculture 2020, 529, 735723. [Google Scholar] [CrossRef]
- Hlophe-Ginindza, S.N.; Moyo, N.A.; Ng’ambi, J.W.; Ncube, I. The effect of exogenous enzyme supplementation on growth performance and digestive enzyme activities in Oreochromis mossambicus fed kikuyu-based diets. Aquac. Res. 2016, 47, 3777–3787. [Google Scholar] [CrossRef]
- Konkit, M.; Kim, W. Activities of amylase, proteinase, and lipase enzymes from Lactococcus chungangensis and its application in dairy products. J. Dairy Sci. 2016, 99, 4999–5007. [Google Scholar] [CrossRef] [Green Version]
- Padmavathi, T.; Bhargavi, R.; Priyanka, P.R.; Niranjan, N.R.; Pavitra, P.V. Screening of potential probiotic lactic acid bacteria and production of amylase and its partial purification. J. Genet. Eng. Biotechnol. 2018, 16, 357–362. [Google Scholar] [CrossRef]
- El-Haroun, E.R.; Goda, A.M.A.-S.; Kabir Chowdhury, M.A. Effect of dietary probiotic Biogen® supplementation as a growth promoter on growth performance and feed utilization of Nile tilapia Oreochromis niloticus (L.). Aquac. Res. 2006, 37, 1473–1480. [Google Scholar] [CrossRef]
- Arani, M.M.; Salati, A.P.; Safari, O.; Keyvanshokooh, S. Dietary supplementation effects of Pediococcus acidilactici as probiotic on growth performance, digestive enzyme activities and immunity response in zebrafish (Danio rerio). Aquacult. Nutr. 2019, 25, 854–861. [Google Scholar] [CrossRef]
- Nolasco-Soria, H. Amylase quantification in aquaculture fish studies: A revision of most used procedures and presentation of a new practical protocol for its assessment. Aquaculture 2021, 538, 736536. [Google Scholar] [CrossRef]
- Al-Tameemi, R.; Aldubaikul, A.; Salman, N.A. Comparative study of α-amylase activity in three Cyprinid species of different feeding habits from Southern Iraq. Turk. J. Fish. Aquat. Sci. 2010, 10, 411–414. [Google Scholar] [CrossRef]
- Siezen, R.J.; Kuipers, O.P.; de Vos, W.M. Comparison of lantibiotic gene clusters and encoded proteins. Antonie Van Leeuwenhoek 1996, 69, 171–184. [Google Scholar] [CrossRef] [Green Version]
- Cheigh, C.I.; Pyun, Y.R. Nisin biosynthesis and its properties. Biotechnol. Lett. 2005, 27, 1641–1648. [Google Scholar] [CrossRef]
- Fusieger, A.; Perin, L.M.; Teixeira, C.G.; de Carvalho, A.F.; Nero, L.A. The ability of Lactococcus lactis subsp. lactis bv. diacetylactis strains in producing nisin. Antonie Van Leeuwenhoek 2020, 113, 651–662. [Google Scholar] [CrossRef] [PubMed]
- de Vos, W.M.; Kuipers, O.P.; van der Meer, J.R.; Siezen, R.J. Maturation pathway of nisin and other lantibiotics: Post-translationally modified antimicrobial peptides exported by Gram-positive bacteria. Mol. Microbiol. 1995, 17, 427–437. [Google Scholar] [CrossRef] [Green Version]
- Qiao, M.; Saris, E.J. Evidence for a role of NisT in transport of the lantibiotic nisin produced by Lactococcus lactis N8. FEMS Microbiol. Lett. 1996, 144, 89–93. [Google Scholar] [CrossRef] [PubMed]
- Zendo, T.; Yoneyama, F.; Sonomoto, K. Lactococcal membrane permeabilizing antimicrobial peptides. Appl. Microbiol. Biotechnol. 2010, 88, 1–9. [Google Scholar] [CrossRef]
- Tosukhowong, A.; Zendo, T.; Visessanguan, W.; Roytrakul, S.; Pumpuang, L.; Jaresitthikunchai, J.; Sonomoto, K. Garvieacin Q, a Novel Class II bacteriocin from Lactococcus garvieae BCC 43578. Appl. Environ. Microbiol. 2012, 78, 1619–1623. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hölscher, T.; Görisch, H. Knockout and overexpression of pyrroloquinoline quinone biosynthetic genes in Gluconobacter oxydans 621H. J. Bacteriol. 2006, 188, 7668–7676. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Al-Nayyef, H.; Guyeux, C.; Bahi, J.M. A pipeline for insertion sequence detection and study for bacterial genome. ar**v 2017, ar**v:1706.08267. Available online: https://arxiv.org/pdf/1706.08267 (accessed on 25 December 2021).
- Argov, T.; Azulay, G.; Pasechnek, A.; Stadnyuk, O.; Ran-Sapir, S.; Borokov, I.; Sigal, N.; Herskovits, A.A. Temperate bacteriophages as regulators of host behavior. Curr. Opin. Microbiol. 2017, 38, 1–7. [Google Scholar] [CrossRef]
- Makarova, K.S.; Wolf, Y.I.; Iranzo, J.; Shmakov, S.A.; Alkhnbashi, O.S.; Brouns, S.J.J.; Charpentier, E.; Cheng, D.; Haft, D.H.; Horvath, P.; et al. Evolutionary classification of CRISPR-Cas systems: A burst of class 2 and derived variants. Nat. Rev. Microbiol. 2020, 18, 67–83. [Google Scholar] [CrossRef] [PubMed]
- Imperial, I.C.V.J.; Iban, J.A. Addressing the antibiotic resistance problem with probiotics: Reducing the risk of its double-edged sword effect. Front. Microbiol. 2016, 7, 1983. [Google Scholar] [CrossRef] [PubMed]
- Gueimonde, M.; Sánchez, B.; de los Reyes-Gavilán, C.G.; Margolles, A. Antibiotic resistance in probiotic bacteria. Front. Microbiol. 2013, 4, 202. [Google Scholar] [CrossRef] [Green Version]
- EFSA (European Food Safety Authority). Update of the list of QPS-recommended biological agents intentionally added to food or feed as notified to EFSA 13: Suitability of taxonomic units notified to EFSA until September 2020. EFSA J. 2021, 18, 5965–6021. [Google Scholar]
- Muñoz-Atienza, E.; Gómez-Sala, B.; Araújo, C.; Campanero, C.; del Campo, R.; Hernández, P.E.; Herranz, C.; Cintas, L.M. Antimicrobial activity, antibiotic susceptibility and virulence factors of Lactic Acid Bacteria of aquatic origin intended for use as probiotics in aquaculture. BMC Microbiol. 2013, 13, 15. [Google Scholar] [CrossRef] [Green Version]
- Anokyewaa, M.A.; Amoah, K.; Li, Y.; Lu, Y.; Kuebutornye, F.K.A.; Asiedu, B.; Seidu, I. Prevalence of virulence genes and antibiotic susceptibility of Bacillus used in commercial aquaculture probiotics in China. Aquac. Rep. 2021, 21, 100784. [Google Scholar] [CrossRef]
Analyzed Element | L. cremoris WA2-67 |
---|---|
IS | IS similar/family/origin/length (bp) |
IS981/IS3/Lactococcus lactis/1224 IS-LL6/IS3/Lactococcus lactis/1254 | |
Plasmids | ND a |
Active prophages | ND a |
CRISPR-cas systems b | CRISPR spacers/cas genes/contig |
4/ND/27 |
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2022 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Feito, J.; Contente, D.; Ponce-Alonso, M.; Díaz-Formoso, L.; Araújo, C.; Peña, N.; Borrero, J.; Gómez-Sala, B.; del Campo, R.; Muñoz-Atienza, E.; et al. Draft Genome Sequence of Lactococcus lactis Subsp. cremoris WA2-67: A Promising Nisin-Producing Probiotic Strain Isolated from the Rearing Environment of a Spanish Rainbow Trout (Oncorhynchus mykiss, Walbaum) Farm. Microorganisms 2022, 10, 521. https://doi.org/10.3390/microorganisms10030521
Feito J, Contente D, Ponce-Alonso M, Díaz-Formoso L, Araújo C, Peña N, Borrero J, Gómez-Sala B, del Campo R, Muñoz-Atienza E, et al. Draft Genome Sequence of Lactococcus lactis Subsp. cremoris WA2-67: A Promising Nisin-Producing Probiotic Strain Isolated from the Rearing Environment of a Spanish Rainbow Trout (Oncorhynchus mykiss, Walbaum) Farm. Microorganisms. 2022; 10(3):521. https://doi.org/10.3390/microorganisms10030521
Chicago/Turabian StyleFeito, Javier, Diogo Contente, Manuel Ponce-Alonso, Lara Díaz-Formoso, Carlos Araújo, Nuria Peña, Juan Borrero, Beatriz Gómez-Sala, Rosa del Campo, Estefanía Muñoz-Atienza, and et al. 2022. "Draft Genome Sequence of Lactococcus lactis Subsp. cremoris WA2-67: A Promising Nisin-Producing Probiotic Strain Isolated from the Rearing Environment of a Spanish Rainbow Trout (Oncorhynchus mykiss, Walbaum) Farm" Microorganisms 10, no. 3: 521. https://doi.org/10.3390/microorganisms10030521