The waste generated by cassava starch processing has an ample variety of molecules that can be converted to value-added products. Cassava starch wastewater (CSW) has a high nutritional value and can be used as a substrate in biological processes, in addition to providing microorganisms of biotechnological interest, due to the rich native biota present. Bacteriocins—peptides synthesized by ribosomes—are capable of inactivating or inhibiting the growth of pathogenic bacteria, used to preserve food, and can be isolated from CSW. This study evaluated growth conditions to produce bacteriocins from a lactic acid bacterium Leuconostoc mesenteroides isolated from CSW, using residues from the cassava processing agroindustry as substrate. The experimental planning by Plackett & Burman (PB) was carried out to evaluate the effects of the variable's sucrose, yeast extract, potassium phosphate, magnesium sulfate, and Tween 80, with 15 assays, 36 h of incubation, and agitation at 100 rpm. From these assays, it was verified that only the variables sucrose, yeast extract, and tween 80 were significant at 90%. The results indicated a maximum bacteriocin production of 1990.47 AU/mL (assay 14), COD (chemical oxygen demand) removal efficiency of 59.99% (assay 11), the sugar removal efficiency of 55.89 (assay 14), and production of lactic acid 21.41 g/L (assay 6).
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References
1.
TappibanP, SmithDR, TriwitayakornK, et al.Recent understanding of starch biosynthesis in cassava for quality improvement: A review. Trends Food Sci Technol, 2019; 83:167-180; doi: 10.1016/J.TIFS.2018.11.019.
2.
AraujoGS, SantiagoCS, MoreiraRT, et al.Nutrient removal by Arthrospira platensis cyanobacteria in cassava processing wastewater. J Water Process Eng, 2021; 40:101826; doi: 10.1016/J.JWPE.2020.101826.
3.
AndreaniCL, TonelloTU, MariAG, et al.Impact of operational conditions on development of the hydrogen-Producing microbial consortium in an AnSBBR from cassava wastewater rich in lactic acid. Int J Hydr Energ, 2019; 44(3):1474–1482; doi: 10.1016/J.IJHYDENE.2018.11.155.
4.
SauerM, RussmayerH, GrabherrR, et al.The efficient clade: Lactic acid bacteria for industrial chemical production. Trends Biotechnol, 2017; 35(8):756-769; doi: 10.1016/J.TIBTECH.2017.05.002.
5.
WangM, GaoZ, ZhangY, et al.Lactic acid bacteria as mucosal delivery vehicles: A realistic therapeutic option. Appl Microbiol Biotechnol, 2016; 100(13):5691-5701; doi: 10.1007/s00253-016-7557-x.
6.
ChikindasML, WeeksR, DriderD, et al.Functions and emerging applications of bacteriocins. Curr Opin Biotechnol, 2018; 49:23-28; doi: 10.1016/j.copbio.2017.07.011.
7.
KumariyaR, GarsaAK, RajputYS, et al.Bacteriocins: Classification, synthesis, mechanism of action and resistance development in food spoilage causing bacteria. Microb Pathogen, 2019; 128:171–177; doi: 10.1016/J.MICPATH.2019.01.002.
8.
LeB and YangS-H. Effect of potential probiotic Leuconostoc mesenteroides FB111 in prevention of cholesterol absorption by modulating NPC1L1/PPARα/SREBP-2 pathways in epithelial Caco-2 cells. Int Microbiol, 2018; 1–9; doi: 10.1007/s10123-018-00047-z.
9.
ZhangP, ZhangP, WuJ, et al.Effects of Leuconostoc mesenteroides on physicochemical and microbial succession characterization of soybean paste, Da-Jiang. LWT, 2019; 115; doi: 10.1016/j.lwt.2019.04.029.
10.
KivançM, FundaEG. A functional food: A traditional Tarhana fermentation. Food Sci Technol, 2017; 37(2):269–274; doi: 10.1590/1678-457x.08815.
11.
YiL, DangJ, ZhangL, et al.Purification, characterization and bactericidal mechanism of a broad spectrum bacteriocin with antimicrobial activity against multidrug-resistant strains produced by Lactobacillus coryniformis XN8. Food Control, 2016; 67:53–62; doi: 10.1016/J.FOODCONT.2016.02.008.
12.
MasudaY, OnoH, KitagawaH, et al.Identification and characterization of leucocyclicin q, a novel cyclic bacteriocin produced by Leuconostoc mesenteroides TK41401. Appl Environ Microbiol, 2011; 77(22):8164–8170; doi: 10.1128/AEM.06348-11.
13.
RaniPS and AgrawalR. Effect on cellular membrane fatty acids in the stressed cells of Leuconostoc mesenteroides: A native probiotic lactic acid bacteria. Food Biotechnol, 2008; 22(1):47–63; doi: 10.1080/08905430701863977.
14.
Sayyed Kamaleddin AllameS, DaudH, YusoffF, et al.Isolation, identification and characterization of Leuconostoc mesenteroides as a new probiotic from intestine of Snakehead Fish (Channa Striatus). Afr J Biotechnol, 2012; 11(16):3810–3816; doi: 10.5897/AJB11.1871.
15.
PenidoFCL, PilóFB, Sandes SH deC, et al.Selection of starter cultures for the production of sour cassava starch in a pilot-scale fermentation process. Brazil J Microbiol, 2018; 49(4):823–831; doi: 10.1016/J.BJM.2018.02.001.
16.
Santos CCA doA, AlmeidaTMM, AbeggMA, et al.Microbiological and chemical characteristics of Tarubá, an Indigenous beverage produced from solid cassava fermentation. Food Microbiol, 2015; 49:182–188; doi: 10.1016/j.fm.2015.02.005.
17.
ParlindunganE, DekiwadiaC, JonesOAH. Factors that influence growth and bacteriocin production in Lactiplantibacillus plantarum B21. Process Biochem, 2021; 107:18–26; doi: 10.1016/J.PROCBIO.2021.05.009.
18.
SaboSS, ConvertiA, IchiwakiS, et al.Bacteriocin production by Lactobacillus plantarum ST16Pa in supplemented whey powder formulations. J Dairy Sci, 2019; 102(1):87–99; doi: 10.3168/JDS.2018-14881.
19.
EatonAD, ClesceriLS, GreenbergAE. Standard methods for the examination of water and wastewater. 21th ed. American Public Health Association; 2005.
20.
DuBoisMichel, GillesKA, HamiltonJK, et al.Colorimetric method for determination of sugars and related substances. Anal Chem, 1956; 28(3):350–356; doi: 10.1021/ac60111a017.
21.
VilvertRM. Obtaining bacteriocin from lactic bacteria in wastewater from the cassava starch industry. 2019. 93f. Thesis (Doctorate in Agricultural Engineering) - Graduate Program in Agricultural Engineering, Unioeste - State University of Western Paraná, Cascavel, Brazil.
22.
PelczarMJ, ChanECS, KriegNR. Microbiology: Concepts and applications. 1993;896.
23.
KarlapudiAP, Krupanidhi SE. RR, et al. Plackett-Burman design for screening of process components and their effects on production of lactase by newly isolated Bacillus Sp. VUVD101 strain from dairy effluent. Beni-Suef University J Basic Appl Sci, 2018; 7(4):543–546; doi: 10.1016/j.bjbas.2018.06.006.
24.
AmialiMN, LacroixC, SimardRE. High nisin Z production by Lactococcus lactis UL719 in whey Permeate with aeration. World J Microbiol Biotechnol, 1998; 14(6):887–894; doi: 10.1023/A:1008863111274.
25.
CaboML, MuradoMA, GonzálezM aP., et al.Effects of aeration and pH gradient on nisin production: A mathematical model. Enzym Microb Technol, 2001; 29(4–5):264–273; doi: 10.1016/S0141-0229(01)00378-7.
26.
ChandrapatiS, O'SullivanJD. Procedure for quantifiable assessment of nutritional parameters influencing nisin production by Lactococcus lactis Subsp. Lactis. J Biotechnol, 1998; 63(3):229–233; doi: 10.1016/S0168-1656(98)00090-X.
27.
CheighC-I, ChoiH-J, ParkH, et al.Influence of growth conditions on the production of a nisin-like bacteriocin by Lactococcus lactis Subsp. Lactis A164 isolated from Kimchi. J Biotechnol, 2002; 95(3):225–235; doi: 10.1016/S0168-1656(02)00010-X.
28.
DabaH, LacroixC, HuangJ, et al.Influence of growth conditions on production and activity of Mesenterocin 5 by a strain of Leuconostoc mesenteroides. Appl Microbiol Biotechnol, 1993; 39(2):166–173; doi: 10.1007/BF00228601.
29.
GuerraNP, RuaML, PastranaL. Nutritional factors affecting the production of two bacteriocins from lactic acid bacteria on whey. Int J Food Microbiol, 2001; 70(3):267–281; doi: 10.1016/S0168-1605(01)00551-7.
30.
LiuC, LiuY, LiaoW, et al.Simultaneous production of nisin and lactic acid from cheese whey: Optimization of fermentation conditions through statistically based experimental designs. Appl Biochem Biotechnol, 2004; 113–116:627–38.
31.
LosteinkitC, UchiyamaK, OchiS, et al.Characterization of bacteriocin N15 produced by Enterococcus faecium N15 and cloning of the related genes. J Biosci Bioeng, 2001; 91(4):390–395.
32.
ParenteE, RicciardiA. Production, recovery and purification of bacteriocins from lactic acid bacteria. Appl Microbiol Biotechnol, 1999; 52(5):628–638.
33.
PongtharangkulT, DemirciA. Evaluation of culture medium for nisin production in a repeated-batch biofilm reactor. Biotechnol Progr, 2006; 22(1):217–224; doi: 10.1021/bp050295q.
34.
Şimşek Ö, ÇonAH, AkkoçN, et al.Influence of growth conditions on the nisin production of bioengineered Lactococcus lactis strains. J Ind Microbiol Biotechnol, 2009; 36(4):481–490; doi: 10.1007/s10295-008-0517-4.
35.
Vessoni PennaTC, Faustino JozalaA, De Lencastre NovaesLC, et al.Production of nisin by Lactococcus lactis in media with skimmed milk. Appl Biochem Biotechnol 2005 122:1, 2005; 122(1):619–637; doi: 10.1385/ABAB:122:1-3:0619.
36.
PennaTCV, JozalaAF, GentilleTR, et al.Detection of nisin expression by Lactococcus lactis using two susceptible bacteria to associate the effects of nisin with EDTA. Appl Biochem Biotechnol, 2006; 129(1–3):334–346; doi: 10.1385/ABAB:129:1:334.
37.
PenteadoED, LazaroCZ, SakamotoIK, et al.Influence of seed sludge and pretreatment method on hydrogen production in packed-bed anaerobic reactors. In: Int J Hydrogen Energ, 2013; pp. 6137–6145; doi: 10.1016/j.ijhydene.2013.01.067.
38.
LewisCB and MontvilleTJ. Detection of bacteriocins produced by lactic acid bacteria. J Microbiol Methods, 1991; 13(2):145–150; doi: 10.1016/0167-7012(91)90014-H.
39.
BrombergR, MorenoI, DelboniRR, et al.Características Da Bacteriocina Produzida Por Lactococcus Lactis Ssp. Hordnia e CTC 484 e Seu Efeito Sobre Listeria Monocytogenes Em Carne Bovina. Ciênc Tecnol Aliment, 2006; 26(1):135–144.
40.
Franco-CendejasR, Colín-CastroCA, Hernández-DuránM, et al.Leuconostoc mesenteroides periprosthetic knee infection, an unusual fastidious gram-positive bacteria: A case report. BMC Infectious Diseases, 2017; 17(1); doi: 10.1186/s12879-017-2315-y.
41.
de PaulaAT, Jeronymo-CenevivaAB, TodorovSD, et al.The two faces of Leuconostoc mesenteroides in food systems. Food Reviews International, 2015; 31(2):147–171; doi: 10.1080/87559129.2014.981825.
42.
StilesME. Bacteriocins produced by Leuconostoc species. J Dairy Sci, 1994; 77(9):2718–2724; doi: 10.3168/jds.S0022-0302(94)77214-3.
DjeniNT, BouateninKMJ-P, AssohounNMC, et al.Biochemical and microbial characterization of cassava inocula from the three main attieke production zones in Côte d'Ivoire. Food Control, 2015; 50:133–140; doi: 10.1016/j.foodcont.2014.08.046.
45.
RamosCL, SousaESO de, RibeiroJ, et al.Microbiological and chemical characteristics of Tarubá, an indigenous beverage produced from solid cassava fermentation. Food Microb, 2015; 49:182–188; doi: 10.1016/j.fm.2015.02.005.
46.
OguntoyinboFA and DoddCER. Bacterial dynamics during the spontaneous fermentation of cassava dough in gari production. Food Control, 2010; 21(3):306–312; doi: 10.1016/j.foodcont.2009.06.010.
47.
AhaotuNN, AnyoguA, ObiohaP, et al.Influence of soy fortification on microbial diversity during cassava fermentation and subsequent physicochemical characteristics of garri. Food Microbiol, 2017; 66:165–172; doi: 10.1016/j.fm.2017.04.019.
48.
EdwardVA, HuchM, DortuC, et al.Biomass production and small-scale testing of freeze-dried lactic acid bacteria starter strains for cassava fermentations. Food Control, 2011; 22(3–4):389–395; doi: 10.1016/j.foodcont.2010.09.008.
49.
Huch (née Kostinek) M, HanakA, SpechtI, et al.Use of Lactobacillus strains to start cassava fermentations for gari production. Int J Food Microbiol, 2008; 128(2):258–267; doi: 10.1016/j.ijfoodmicro.2008.08.017.
50.
AnyoguA, AwamariaB, SutherlandJP, et al.Molecular characterisation and antimicrobial activity of bacteria associated with submerged lactic acid cassava fermentation. Food Control, 2014; 39(1):119–127; doi: 10.1016/j.foodcont.2013.11.005.
51.
CoulinP, FarahZ, AssanvoJ, et al.Characterisation of the microflora of Attiéké, a fermented cassava product, during traditional small-scale preparation. Int J Food Microbiol, 2006; 106(2):131–136; doi: 10.1016/j.ijfoodmicro.2005.06.012.
52.
AmpeF, SirventA, ZakhiaN. Dynamics of the microbial community responsible for traditional sour cassava starch fermentation studied by denaturing gradient gel electrophoresis and quantitative RRNA hybridization. Int J Food Microbiol, 2001; 65(1–2):45–54; doi: 10.1016/S0168-1605(00)00502-X.
53.
LeiV, Amoa-AwuaWKA, BrimerL. Degradation of cyanogenic glycosides by Lactobacillus plantarum strains from spontaneous cassava fermentation and other microorganisms. Int J Food Microbiol, 1999; 53(2–3):169–184; doi: 10.1016/S0168-1605(99)00156-7.
54.
Omar NBen, AmpeF, RaimbaultM, et al.Molecular diversity of lactic acid bacteria from cassava sour starch (Colombia). Systematic Appl Microbiol, 2000; 23(2):285–291; doi: 10.1016/S0723-2020(00)80016-8.
55.
MalheirosPS, Sant'AnnaV, TodorovSD, et al.Optimization of growth and bacteriocin production by Lactobacillus sakei Subsp. Sakei 2a. Brazil J Microbiol, 2015; 46(3):825–834; doi: 10.1590/S1517-838246320140279.
56.
MartinezFAC, BalciunasEM, ConvertiA, et al.Bacteriocin production by Bifidobacterium Spp. A Review. Biotechnol Adv, 2013; 31(4):482–488; doi: 10.1016/j.biotechadv.2013.01.010.
57.
RosaCM, FrancoBDGM, MontvilleTJ, et al.Purification and mechanistic action of a bacteriocin produced by a Brazilian Sausage Isolate, Lactobacillus Sake 2a. J Food Safety, 2002; 22(1):39–54; doi: 10.1111/j.1745-4565.2002.tb00329.x.
58.
AbbasiliasiS, TanJS, Tengku IbrahimTA, et al.Fermentation factors influencing the production of bacteriocins by lactic acid bacteria: A review. RSC Adv, 2017; 7(47):29395–29420; doi: 10.1039/c6ra24579j.
59.
WayahSB, PhilipK. Characterization, yield optimization, scale up and biopreservative potential of fermencin SA715, a novel bacteriocin from Lactobacillus fermentum GA715 of goat milk origin. Microbial Cell Factories, 2018; 17(1):1–18; doi: 10.1186/s12934-018-0972-1.
60.
MataragasM, DrosinosEH, TsakalidouE, et al.Influence of nutrients on growth and bacteriocin production by Leuconostoc mesenteroides L124 and Lactobacillus curvatus L442. Antonie van Leeuwenhoek Int J General Molecular Microbiol, 2004; 85(3):191–198; doi: 10.1023/B:ANTO.0000020291.01957.a2.
61.
PapagianniM, AvramidisN, FiliousisG. investigating the relationship between the specific glucose uptake rate and nisin production in aerobic batch and fed-batch glucostat cultures of Lactococcus lactis. Enzym Microb Technol, 2007; 40(6):1557–1563; doi: 10.1016/j.enzmictec.2006.10.035.
62.
FurtadoDN, TodorovSD, LandgrafM, et al.Bacteriocinogenic Lactococcus lactis Subsp. Lactis DF04MI isolated from goat milk: Characterization of the bacteriocin. Brazil J Microbiol, 2014; 45(4):1541–1550; doi: 10.1590/S1517-83822014000400052.
63.
TeófiloRF, FerreiraMMC. Quimiometria II: Planilhas Eletrônicas Para Cálculus de Planejamentos Experimentais, Um Tutorial. Quimica Nova, 2006; 29(2):338–350; doi: 10.1590/s0100-40422006000200026.
64.
CamposAT, DagaJ, RodriguesEE, et al.Tratamento de Águas Residuárias de Fecularia Por Meio de Lagoas de Estabilização. Engenharia Agricola, 2006; 26(1):235–242; doi: 10.1590/s0100-69162006000100026.
65.
CárdenasN, LaiñoJE, DelgadoS, et al.Relationships between the genome and some phenotypical properties of Lactobacillus fermentum CECT 5716, a probiotic strain isolated from human milk. Appl Microbiol Biotechnol, 2015; 99(10):4343–53; doi: 10.1007/s00253-015-6429-0.
66.
PizatoS, OgrodowskiCS, Prentice-HernándezC. Screening de Variáveis Para a Produção de Biomassa e Ácido Lático Utilizando Planejamento Plackett-Burman. J Bioenerg Food Sci, 2015; 2(3):117–128; doi: 10.1806/7/jbfs.v2i3.38.
