Generic placeholder image

Protein & Peptide Letters

Editor-in-Chief

ISSN (Print): 0929-8665
ISSN (Online): 1875-5305

Mini-Review Article

Putative Antimicrobial Peptides in Fish: Using Zebrafish as a Representative

Author(s): Xiyang Chen, Yunhai Yi, Chao Bian, Xinxin You and Qiong Shi*

Volume 27, Issue 11, 2020

Page: [1059 - 1067] Pages: 9

DOI: 10.2174/0929866527666200517104610

Price: $65

conference banner
Abstract

Antimicrobial peptides (AMPs) are a group of short peptides in vertebrates, independently or derived from big proteins (AMP precursors), for innate immune adaptation to fight against exogenous pathogens. Therefore, they provide attractive templates for us to develop new alternatives to antibiotics, which will relieve the threats of microbial resistance and drug residual. Fish reside in various environments; however, AMP research in fish have long been lagged behind. These highly diverse peptides in fish, regardless whether they are digested from proteins or not, constitute a sophisticate line for host defense. Exploring AMPs’ detailed composition in fish will benefit us with a better understanding of them in vertebrates. This mini-review presents brief descriptions of AMPs and their research advances in fish, using zebrafish as the representative and comparing this model fish with well-studied amphibious mudskippers and tetraploid Atlantic salmon. Common features and species-specific characteristics among various fish provide valuable genetic resources for high-throughput development of novel antibiotic alternatives. In addition, the diversity and heterogeneity in tissue distribution also revealed the complex synergism of AMPs/AMP precursors. These big datasets of genomes and transcriptomes lay a solid foundation for theoretic researches and practical applications of AMPs in fish aquaculture and drug development.

Keywords: Antimicrobial peptide, zebrafish, high-throughput identification, genome, transcriptome, tissue distribution.

Next »
Graphical Abstract

[1]
Wang, K.; Jia, F.; Dang, W.; Zhao, Y.; Zhu, R.; Sun, M.; Qiu, S.; An, X.; Ma, Z.; Zhu, Y.; Yan, J.; Kong, Z.; Yan, W.; Wang, R. Antifungal effect and action mechanism of antimicrobial peptide polybia-CP. J. Pept. Sci., 2016, 22(1), 28-35.
[http://dx.doi.org/10.1002/psc.2835] [PMID: 26680221]
[2]
Methatham, T.; Boonchuen, P.; Jaree, P.; Tassanakajon, A.; Somboonwiwat, K. Antiviral action of the antimicrobial peptide ALFPm3 from Penaeus monodon against white spot syndrome virus. Dev. Comp. Immunol., 2017, 69, 23-32.
[http://dx.doi.org/10.1016/j.dci.2016.11.023] [PMID: 27919648]
[3]
Hoskin, D.W.; Ramamoorthy, A. Studies on anticancer activities of antimicrobial peptides. Biochim. Biophys. Acta, 2008, 1778(2), 357-375.
[http://dx.doi.org/10.1016/j.bbamem.2007.11.008] [PMID: 18078805]
[4]
Mansour, S.C.; Pena, O.M.; Hancock, R.E. Host defense peptides: Front-line immunomodulators. Trends Immunol., 2014, 35(9), 443-450.
[http://dx.doi.org/10.1016/j.it.2014.07.004] [PMID: 25113635]
[5]
Hilchie, A.L.; Wuerth, K.; Hancock, R.E. Immune modulation by multifaceted cationic host defense (antimicrobial) peptides. Nat. Chem. Biol., 2013, 9(12), 761-768.
[http://dx.doi.org/10.1038/nchembio.1393] [PMID: 24231617]
[6]
Haney, E.F.; Hancock, R.E. Peptide design for antimicrobial and immunomodulatory applications. Biopolymers, 2013, 100(6), 572-583.
[http://dx.doi.org/10.1002/bip.22250] [PMID: 23553602]
[7]
Hancock, R.E.; Haney, E.F.; Gill, E.E. The immunology of host defence peptides: Beyond antimicrobial activity. Nat. Rev. Immunol., 2016, 16(5), 321-334.
[http://dx.doi.org/10.1038/nri.2016.29] [PMID: 27087664]
[8]
Li, W.; Tailhades, J.; O’Brien-Simpson, N.M.; Separovic, F.; Otvos, L., Jr; Hossain, M.A.; Wade, J.D. Proline-rich antimicrobial peptides: Potential therapeutics against antibiotic-resistant bacteria. Amino Acids, 2014, 46(10), 2287-2294.
[http://dx.doi.org/10.1007/s00726-014-1820-1] [PMID: 25141976]
[9]
Haney, E.F.; Mansour, S.C.; Hancock, R.E. Antimicrobial peptides: An introduction. Methods Mol. Biol., 2017, 1548, 3-22.
[http://dx.doi.org/10.1007/978-1-4939-6737-7_1] [PMID: 28013493]
[10]
Nuti, R.; Goud, N.S.; Saraswati, A.P.; Alvala, R.; Alvala, M. Antimicrobial Peptides: A promising therapeutic strategy in tackling antimicrobial resistance. Curr. Med. Chem., 2017, 24(38), 4303-4314.
[http://dx.doi.org/10.2174/0929867324666170815102441] [PMID: 28814242]
[11]
Okocha, R.C.; Olatoye, I.O.; Adedeji, O.B. Food safety impacts of antimicrobial use and their residues in aquaculture. Public Health Rev., 2018, 39, 21.
[http://dx.doi.org/10.1186/s40985-018-0099-2] [PMID: 30094087]
[12]
Ojha, S.; Deep, S.; Kundu, S. Plant derived antimicrobial peptide Ib-AMP1 as a potential alternative drug candidate for Staphylococcus aureus toxins. Cell. Mol. Biol., 2017, 63(6), 52-55.
[http://dx.doi.org/10.14715/cmb/2017.63.6.11] [PMID: 28968210]
[13]
Pan, C.Y.; Chen, J.Y.; Lin, T.L.; Lin, C.H. In vitro activities of three synthetic peptides derived from epinecidin-1 and an anti-lipopolysaccharide factor against Propionibacterium acnes, Candida albicans, and Trichomonas vaginalis. Peptides, 2009, 30(6), 1058-1068.
[http://dx.doi.org/10.1016/j.peptides.2009.02.006] [PMID: 19463737]
[14]
Koo, H.; Seo, J. Antimicrobial peptides under clinical investigation. Pept Sci, 2019, 111, e24122.
[http://dx.doi.org/10.1002/pep2.24122]
[15]
Jenssen, H.; Hamill, P.; Hancock, R.E. Peptide antimicrobial agents. Clin. Microbiol. Rev., 2006, 19(3), 491-511.
[http://dx.doi.org/10.1128/CMR.00056-05] [PMID: 16847082]
[16]
Waghu, F.H.; Gopi, L.; Barai, R.S.; Ramteke, P.; Nizami, B.; Idicula-Thomas, S. CAMP: Collection of sequences and structures of antimicrobial peptides. Nucleic Acids Res., 2014, 42(Database issue), D1154-D1158.
[http://dx.doi.org/10.1093/nar/gkt1157] [PMID: 24265220]
[17]
Wang, G.; Li, X.; Wang, Z. APD3: The antimicrobial peptide database as a tool for research and education. Nucleic Acids Res., 2016, 44(D1), D1087-D1093.
[http://dx.doi.org/10.1093/nar/gkv1278] [PMID: 26602694]
[18]
Shai, Y. Mode of action of membrane active antimicrobial peptides. Biopolymers, 2002, 66(4), 236-248.
[http://dx.doi.org/10.1002/bip.10260] [PMID: 12491537]
[19]
Falanga, A.; Lombardi, L.; Franci, G.; Vitiello, M.; Iovene, M.R.; Morelli, G.; Galdiero, M.; Galdiero, S. Marine antimicrobial peptides: Nature provides templates for the design of novel compounds against pathogenic bacteria. Int. J. Mol. Sci., 2016, 17(5), 785.
[http://dx.doi.org/10.3390/ijms17050785] [PMID: 27213366]
[20]
Nguyen, L.T.; Haney, E.F.; Vogel, H.J. The expanding scope of antimicrobial peptide structures and their modes of action. Trends Biotechnol., 2011, 29(9), 464-472.
[http://dx.doi.org/10.1016/j.tibtech.2011.05.001] [PMID: 21680034]
[21]
Hancock, R.E.; Lehrer, R. Cationic peptides: A new source of antibiotics. Trends Biotechnol., 1998, 16(2), 82-88.
[http://dx.doi.org/10.1016/S0167-7799(97)01156-6] [PMID: 9487736]
[22]
Nicolas, P. Multifunctional host defense peptides: Intracellular-targeting antimicrobial peptides. FEBS J., 2009, 276(22), 6483-6496.
[http://dx.doi.org/10.1111/j.1742-4658.2009.07359.x] [PMID: 19817856]
[23]
Powers, J.P.; Hancock, R.E. The relationship between peptide structure and antibacterial activity. Peptides, 2003, 24(11), 1681-1691.
[http://dx.doi.org/10.1016/j.peptides.2003.08.023] [PMID: 15019199]
[24]
Bouchet, P.; Duarte, C.M. The exploration of marine biodiversity: Scientific and technological challenges. Fundación BBVA, 2006, 33, 1-34.
[25]
Hoang, V.L.; Kim, S.K. Antimicrobial peptides from marine sources. Curr. Protein Pept. Sci., 2013, 14(3), 205-211.
[http://dx.doi.org/10.2174/13892037113149990037] [PMID: 23721311]
[26]
Primor, N.; Tu, A.T. Conformation of pardaxin, the toxin of the flatfish Pardachirus marmoratus. Biochim. Biophys. Acta, 1980, 626(2), 299-306.
[http://dx.doi.org/10.1016/0005-2795(80)90124-5] [PMID: 7213649]
[27]
Liu, J.; Jiang, J.; Wu, Z.; Xie, F. Antimicrobial peptides from the skin of the Asian frog, Odorrana jingdongensis: De novo sequencing and analysis of tandem mass spectrometry data. J. Proteomics, 2012, 75(18), 5807-5821.
[http://dx.doi.org/10.1016/j.jprot.2012.08.004] [PMID: 22917879]
[28]
Yi, Y.; You, X.; Bian, C.; Chen, S.; Lv, Z.; Qiu, L.; Shi, Q. High-throughput identification of antimicrobial peptides from amphibious mudskippers. Mar. Drugs, 2017, 15(11), 364.
[http://dx.doi.org/10.3390/md15110364] [PMID: 29165344]
[29]
Wang, D.; Chen, X.; Zhang, X.; Li, J.; Yi, Y.; Bian, C.; Shi, Q.; Lin, H.; Li, S.; Zhang, Y.; You, X. Whole genome sequencing of the giant grouper (Epinephelus lanceolatus) and high-throughput screening of putative antimicrobial peptide genes. Mar. Drugs, 2019, 17(9), 503.
[http://dx.doi.org/10.3390/md17090503] [PMID: 31466296]
[30]
Katzenback, B.A. Antimicrobial peptides as mediators of innate immunity in teleosts. Biology (Basel), 2015, 4(4), 607-639.
[http://dx.doi.org/10.3390/biology4040607] [PMID: 26426065]
[31]
Chuah, L.O.; Effarizah, M.E.; Goni, A.M.; Rusul, G. Antibiotic application and emergence of multiple antibiotic resistance (MAR) in global catfish aquaculture. Curr. Environ. Health Rep., 2016, 3(2), 118-127.
[http://dx.doi.org/10.1007/s40572-016-0091-2] [PMID: 27038482]
[32]
Fang, H.; Huang, K.; Yu, J.; Ding, C.; Wang, Z.; Zhao, C.; Yuan, H.; Wang, Z.; Wang, S.; Hu, J.; Cui, Y. Metagenomic analysis of bacterial communities and antibiotic resistance genes in the Eriocheir sinensis freshwater aquaculture environment. Chemosphere, 2019, 224, 202-211.
[http://dx.doi.org/10.1016/j.chemosphere.2019.02.068] [PMID: 30822726]
[33]
Pan, C.Y.; Chen, J.Y.; Cheng, Y.S.; Chen, C.Y.; Ni, I.H.; Sheen, J.F.; Pan, Y.L.; Kuo, C.M. Gene expression and localization of the epinecidin-1 antimicrobial peptide in the grouper (Epinephelus coioides), and its role in protecting fish against pathogenic infection. DNA Cell Biol., 2007, 26(6), 403-413.
[http://dx.doi.org/10.1089/dna.2006.0564] [PMID: 17570764]
[34]
Jheng, Y.H.; Lee, L.H.; Ting, C.H.; Pan, C.Y.; Hui, C.F.; Chen, J.Y. Zebrafish fed on recombinant Artemia expressing epinecidin-1 exhibit increased survival and altered expression of immunomodulatory genes upon Vibrio vulnificus infection. Fish Shellfish Immunol., 2015, 42(1), 1-15.
[http://dx.doi.org/10.1016/j.fsi.2014.10.019] [PMID: 25462461]
[35]
Ting, C.H.; Chen, Y.C.; Chen, J.Y. Nile tilapia fry fed on antimicrobial peptide Epinecidin-1-expressing Artemia cyst exhibit enhanced immunity against acute bacterial infection. Fish Shellfish Immunol., 2018, 81, 37-48.
[http://dx.doi.org/10.1016/j.fsi.2018.07.008] [PMID: 29981882]
[36]
Pan, C.Y.; Huang, T.C.; Wang, Y.D.; Yeh, Y.C.; Hui, C.F.; Chen, J.Y. Oral administration of recombinant epinecidin-1 protected grouper (Epinephelus coioides) and zebrafish (Danio rerio) from Vibrio vulnificus infection and enhanced immune-related gene expressions. Fish Shellfish Immunol., 2012, 32(6), 947-957.
[http://dx.doi.org/10.1016/j.fsi.2012.01.023] [PMID: 22554570]
[37]
Álvarez, C.A.; Acosta, F.; Montero, D.; Guzmán, F.; Torres, E.; Vega, B.; Mercado, L. Synthetic hepcidin from fish: Uptake and protection against Vibrio anguillarum in sea bass (Dicentrarchus labrax). Fish Shellfish Immunol., 2016, 55, 662-670.
[http://dx.doi.org/10.1016/j.fsi.2016.06.035] [PMID: 27368538]
[38]
Masso-Silva, J.A.; Diamond, G. Antimicrobial peptides from fish. Pharmaceuticals (Basel), 2014, 7(3), 265-310.
[http://dx.doi.org/10.3390/ph7030265] [PMID: 24594555]
[39]
Kościuczuk, E.M.; Lisowski, P.; Jarczak, J.; Strzałkowska, N.; Jóźwik, A.; Horbańczuk, J.; Krzyżewski, J.; Zwierzchowski, L.; Bagnicka, E. Cathelicidins: Family of antimicrobial peptides. A review. Mol. Biol. Rep., 2012, 39(12), 10957-10970.
[http://dx.doi.org/10.1007/s11033-012-1997-x] [PMID: 23065264]
[40]
Bian, C.; Li, J.; Lin, X.; Chen, X.; Yi, Y.; You, X.; Zhang, Y.; Lv, Y.; Shi, Q. Whole genome sequencing of the blue tilapia (Oreochromis aureus) provides a valuable genetic resource for biomedical research on tilapias. Mar. Drugs, 2019, 17(7), 386.
[http://dx.doi.org/10.3390/md17070386] [PMID: 31261751]
[41]
Agerberth, B.; Boman, A.; Andersson, M.; Jörnvall, H.; Mutt, V.; Boman, H.G. Isolation of three antibacterial peptides from pig intestine: Gastric inhibitory polypeptide (7-42), diazepam-binding inhibitor (32-86) and a novel factor, peptide 3910. Eur. J. Biochem., 1993, 216(2), 623-629.
[http://dx.doi.org/10.1111/j.1432-1033.1993.tb18182.x] [PMID: 8375398]
[42]
Choi, H.; Hwang, J.S.; Lee, D.G. Identification of a novel antimicrobial peptide, scolopendin 1, derived from centipede Scolopendra subspinipes mutilans and its antifungal mechanism. Insect Mol. Biol., 2014, 23(6), 788-799.
[http://dx.doi.org/10.1111/imb.12124] [PMID: 25209888]
[43]
Eslamloo, K.; Xue, X.; Hall, J.R.; Smith, N.C.; Caballero-Solares, A.; Parrish, C.C.; Taylor, R.G.; Rise, M.L. Transcriptome profiling of antiviral immune and dietary fatty acid dependent responses of Atlantic salmon macrophage-like cells. BMC Genomics, 2017, 18(1), 706.
[http://dx.doi.org/10.1186/s12864-017-4099-2] [PMID: 28886690]
[44]
You, X.; Bian, C.; Zan, Q.; Xu, X.; Liu, X.; Chen, J.; Wang, J.; Qiu, Y.; Li, W.; Zhang, X.; Sun, Y.; Chen, S.; Hong, W.; Li, Y.; Cheng, S.; Fan, G.; Shi, C.; Liang, J.; Tom Tang, Y.; Yang, C.; Ruan, Z.; Bai, J.; Peng, C.; Mu, Q.; Lu, J.; Fan, M.; Yang, S.; Huang, Z.; Jiang, X.; Fang, X.; Zhang, G.; Zhang, Y.; Polgar, G.; Yu, H.; Li, J.; Liu, Z.; Zhang, G.; Ravi, V.; Coon, S.L.; Wang, J.; Yang, H.; Venkatesh, B.; Wang, J.; Shi, Q. Mudskipper genomes provide insights into the terrestrial adaptation of amphibious fishes. Nat. Commun., 2014, 5, 5594.
[http://dx.doi.org/10.1038/ncomms6594] [PMID: 25463417]
[45]
Noga, E.J.; Ullal, A.J.; Corrales, J.; Fernandes, J.M. Application of antimicrobial polypeptide host defenses to aquaculture: Exploitation of downregulation and upregulation responses. Comp. Biochem. Physiol. Part D Genomics Proteomics, 2011, 6(1), 44-54.
[http://dx.doi.org/10.1016/j.cbd.2010.06.001] [PMID: 20584633]
[46]
Noga, E.J.; Fan, Z.; Silphaduang, U. Histone-like proteins from fish are lethal to the parasitic dinoflagellate Amyloodinium ocellatum. Parasitology, 2001, 123(Pt 1), 57-65.
[http://dx.doi.org/10.1017/S0031182001007971] [PMID: 11467783]
[47]
Robinette, D.; Wada, S.; Arroll, T.; Levy, M.G.; Miller, W.L.; Noga, E.J. Antimicrobial activity in the skin of the channel catfish Ictalurus punctatus: Characterization of broad-spectrum histone-like antimicrobial proteins. Cell. Mol. Life Sci., 1998, 54(5), 467-475.
[http://dx.doi.org/10.1007/s000180050175] [PMID: 9645227]
[48]
Chang, C.I.; Zhang, Y.A.; Zou, J.; Nie, P.; Secombes, C.J. Two cathelicidin genes are present in both rainbow trout (Oncorhynchus mykiss) and atlantic salmon (Salmo salar). Antimicrob. Agents Chemother., 2006, 50(1), 185-195.
[http://dx.doi.org/10.1128/AAC.50.1.185-195.2006] [PMID: 16377685]
[49]
Broekman, D.C.; Guðmundsson, G.H.; Maier, V.H. Differential regulation of cathelicidin in salmon and cod. Fish Shellfish Immunol., 2013, 35(2), 532-538.
[http://dx.doi.org/10.1016/j.fsi.2013.05.005] [PMID: 23727282]
[50]
Lu, X.J.; Chen, J.; Huang, Z.A.; Shi, Y.H.; Lv, J.N. Identification and characterization of a novel cathelicidin from ayu, Plecoglossus altivelis. Fish Shellfish Immunol., 2011, 31(1), 52-57.
[http://dx.doi.org/10.1016/j.fsi.2011.03.005] [PMID: 21397030]
[51]
Arenas, G.; Guzmán, F.; Cárdenas, C.; Mercado, L.; Marshall, S.H. A novel antifungal peptide designed from the primary structure of a natural antimicrobial peptide purified from Argopecten purpuratus hemocytes. Peptides, 2009, 30(8), 1405-1411.
[http://dx.doi.org/10.1016/j.peptides.2009.05.019] [PMID: 19481126]
[52]
Wagner, G.P.; Kin, K.; Lynch, V.J. Measurement of mRNA abundance using RNA-seq data: RPKM measure is inconsistent among samples. Theory Biosci., 2012, 131(4), 281-285.
[http://dx.doi.org/10.1007/s12064-012-0162-3] [PMID: 22872506]
[53]
Pasquier, J.; Cabau, C.; Nguyen, T.; Jouanno, E.; Severac, D.; Braasch, I.; Journot, L.; Pontarotti, P.; Klopp, C.; Postlethwait, J.H.; Guiguen, Y.; Bobe, J. Gene evolution and gene expression after whole genome duplication in fish: The PhyloFish database. BMC Genomics, 2016, 17, 368.
[http://dx.doi.org/10.1186/s12864-016-2709-z] [PMID: 27189481]
[54]
Bishop, B.M.; Juba, M.L.; Russo, P.S.; Devine, M.; Barksdale, S.M.; Scott, S.; Settlage, R.; Michalak, P.; Gupta, K.; Vliet, K.; Schnur, J.M.; van Hoek, M.L. Discovery of novel antimicrobial peptides from Varanus komodoensis (Komodo Dragon) by large-scale analyses and de-novo-assisted sequencing using electron-transfer dissociation mass spectrometry. J. Proteome Res., 2017, 16(4), 1470-1482.
[http://dx.doi.org/10.1021/acs.jproteome.6b00857] [PMID: 28164707]
[55]
Chen, X.; Yi, Y.; You, X.; Liu, J.; Shi, Q. High-throughput identification of putative antimicrobial peptides from multi-omics data of the lined seahorse (Hippocampus erectus). Mar. Drugs, 2019, 18(1), 30.
[http://dx.doi.org/10.3390/md18010030] [PMID: 31905755]
[56]
Lin, Q.; Fan, S.; Zhang, Y.; Xu, M.; Zhang, H.; Yang, Y.; Lee, A.P.; Woltering, J.M.; Ravi, V.; Gunter, H.M.; Luo, W.; Gao, Z.; Lim, Z.W.; Qin, G.; Schneider, R.F.; Wang, X.; Xiong, P.; Li, G.; Wang, K.; Min, J.; Zhang, C.; Qiu, Y.; Bai, J.; He, W.; Bian, C.; Zhang, X.; Shan, D.; Qu, H.; Sun, Y.; Gao, Q.; Huang, L.; Shi, Q.; Meyer, A.; Venkatesh, B. The seahorse genome and the evolution of its specialized morphology. Nature, 2016, 540(7633), 395-399.
[http://dx.doi.org/10.1038/nature20595] [PMID: 27974754]
[57]
Melamed, P.; Xue, Y.; Poon, J.F.; Wu, Q.; Xie, H.; Yeo, J.; Foo, T.W.; Chua, H.K. The male seahorse synthesizes and secretes a novel C-type lectin into the brood pouch during early pregnancy. FEBS J., 2005, 272(5), 1221-1235.
[http://dx.doi.org/10.1111/j.1742-4658.2005.04556.x] [PMID: 15720396]
[58]
Tessera, V.; Guida, F.; Juretić, D.; Tossi, A. Identification of antimicrobial peptides from teleosts and anurans in expressed sequence tag databases using conserved signal sequences. FEBS J., 2012, 279(5), 724-736.
[http://dx.doi.org/10.1111/j.1742-4658.2011.08463.x] [PMID: 22188679]
[59]
Gabere, M.N.; Noble, W.S. Empirical comparison of web-based antimicrobial peptide prediction tools. Bioinformatics, 2017, 33(13), 1921-1929.
[http://dx.doi.org/10.1093/bioinformatics/btx081] [PMID: 28203715]
[60]
Veltri, D.; Kamath, U.; Shehu, A. Deep learning improves antimicrobial peptide recognition. Bioinformatics, 2018, 34(16), 2740-2747.
[http://dx.doi.org/10.1093/bioinformatics/bty179] [PMID: 29590297]
[61]
Makowski, M.; Silva, I.C.; Pais do Amaral, C.; Gonçalves, S.; Santos, N.C. Advances in lipid and metal nanoparticles for antimicrobial peptide delivery. Pharmaceutics, 2019, 11(11), 588.
[http://dx.doi.org/10.3390/pharmaceutics11110588] [PMID: 31717337]
[62]
Dong, B.; Yi, Y.; Liang, L.; Shi, Q. High throughput identification of antimicrobial peptides from fish gastrointestinal microbiota. Toxins (Basel), 2017, 9(9), 266.
[http://dx.doi.org/10.3390/toxins9090266] [PMID: 28867788]
[63]
Settanni, L.; Corsetti, A. Application of bacteriocins in vegetable food biopreservation. Int. J. Food Microbiol., 2008, 121(2), 123-138.
[http://dx.doi.org/10.1016/j.ijfoodmicro.2007.09.001] [PMID: 18022269]

Rights & Permissions Print Cite
© 2024 Bentham Science Publishers | Privacy Policy