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http://dx.doi.org/10.7853/kjvs.2017.40.2.119

Characteristics of digestive enzyme activity, antibiotic resistance, and pathogenicity of bacteria inhabited in animal feed resources  

Yi, Kwon Jung (Department of Animal Science and Technology, Konkuk University)
Cho, Sang Seop (Yangjucity Agricultural Technology Center)
Kim, Soo-Ki (Department of Animal Science and Technology, Konkuk University)
Publication Information
Korean Journal of Veterinary Service / v.40, no.2, 2017 , pp. 119-131 More about this Journal
Abstract
Among different types of spoilage, microbial contamination can cause feed decomposition, which results in decreases in feed intake and productivity, infection, and breeding disorder. During the storage time, various microbes have a chance to inoculate with depreciation of feed and to infect the animals. We investigated bacteria that inhabit diverse feed ingredients and complete feed which have been stored for a few months. We isolated and identified 30 genera and 62 species of bacteria. Among these 62 species, 21 species were of non-pathogenic bacteria, 18 species were of pathogenic bacteria, 9 species were of opportunistic pathogens, and 14 species were of unknown bacteria. Pantoea allii and 24 species showed proteolytic enzyme activity. We also confirmed that 6 species including Pseudomonas psychrotolerans showed ${\alpha}$-amylase activity, and 29 species including Burkholderia vietnamiensis showed cellulase activity. Microbacterium testaceum and 3 species showed resistance to Ampicillin, Kanamycin, Streptomycin, Gentamicin, Carbenicillin, and Erythromycin ($50{\mu}g/mL$). Using mealworm larvae (Tenebrio molitor L.) as a model for pathogenicity, we confirmed that 8 species including Staphylococcus xylosus had pathogenicity for mealworm larvae. Especially, Enterobacter hormaechei, Staphylococcus xylosus, and Staphylococcus hominis were reported as being pathogenic for humans. This research suggests that hygienic management of animal feed is essential because beneficial and harmful bacteria can inhabit animal feed differently during storage and distribution.
Keywords
Antibacterial resistance; Bacteria; Enzyme activity; Feed; Pathogenicity;
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1 Shin GW, You MJ, Lee HS, Lee CS. 2012. Catheter-related bacteremia caused by multidrug-resistant Leclercia adecarboxylata in a patient with breast cancer. J Clin Microbiol 50: 3129-3132.   DOI
2 Shivaji S, Chaturvedi P, Begum Z, Pindi PK, Manorama R, Padmanaban DA, Shouche YS, Pawar S, Vaishampayan P, Dutt CB, Datta GN, Manchanda RK, Rao UR, Bhargava PM, Narlikar JV. 2009. Janibacter hoylei sp. nov., Bacillus isronensis sp. nov. and Bacillus aryabhattai sp. nov., isolated from cryotubes used for collecting air from the upper atmosphere. Int J Syst Evol Microbiol 59: 2977-2986.   DOI
3 Sillankorva S, Neubauer P, Azeredo J. 2010. Phage control of dual species biofilms of Pseudomonas fluorescens and Staphylococcus lentus. Biofouling 26: 567-575.   DOI
4 Top J, Willems R, Bonten M. 2008. Emergence of CC17 Enterococcus faecium: from commensal to hospital-adapted pathogen. FEMS Immunol Med Microbiol 52: 297-308.
5 Treichel H, De Oliveira D, Mazutti MA, Luccio MD, Oliveira JV. 2009. A review on Microbial lipases production. Food Bioprocess Technol 3: 182-196.
6 Triplett LR, Verdier V, Campillo T, Malderghem CV, Cleenwerch I, Maes M, Deblais L, Corral R, Koita O, Cottyn B, Leach JE. 2015. Characterization of a novel clade of Xanthomonas isolated from rice leaves in Mali and proposal of Xanthomonas maliensis sp. nov. Antonie van Leeuwenhoek 107: 869-881.   DOI
7 Turgis M, Vu KD, Millette M, Dupont C, Lacroix M. 2016. Influence of Environmental Factors on Bacteriocin Production by Human Isolates of Lactococcus lactis MM19 and Pediococcus acidilactici MM33. Probiotics Antimicrob Proteins 8: 53-59.   DOI
8 Vaikuntapu PR, Dutta S, Samudrala RB, Rao VRVN, Kalam S, Podile AR. 2014. Preferential promotion of Lycopersicon esculentum (Tomato) growth by plant growth promoting bacteria associated with tomato. Indian J Microbiol 54: 403-412.   DOI
9 Brooke JS. 2012. Stenotrophomonas maltophilia: an emerging global opportunistic pathogen. Clin Microbiol Rev 25: 2-41.   DOI
10 Brady CL, Goszczynska T, Venter SN, Cleenwerck I, De Vos P, Gitaitis RD, Coutinho TA. 2011. Pantoea allii sp. nov., isolated from onion plants and seed. Int J Syst Evol Microbiol 61: 932-937.   DOI
11 Casaburi A, Di Martino V, Ferranti P, Picariello L, Villani F, 2016. Technological properties and bacteriocins production by Lactobacillus curvatus 54M16 and its use as starter culture for fermented sausage manufacture. Food Control 59: 31-45.   DOI
12 Srinivasan S, Kim HS, Kim MK, Lee M. 2012. Pseudoclavibacter caeni sp. nov., isolated from sludge of a sewage disposal plant. Int J Syst Evol Microbiol 62: 786-790.   DOI
13 Lamichhane JR, Varvaro L, Balestra GM. 2010. Bacterial leaf spot caused by Xanthomonas cucurbitae reported on pumpkin in Nepal. New Disease Reports 22: 20.   DOI
14 Iha MH, Barbosa CB, Okada IA, Trucksess MW. 2013. Aflatoxin M1 in milk and distribution and stability of aflatoxin $M_1$ during production and storage of yoghurt and cheese. Food Control 29: 1-6.   DOI
15 Li S, Zhao Y, Zhang L, Zhang X, Huang L, Li D, Niu C, Yang Z, Wang Q. 2012. Antioxidant activity of Lactobacillus plantarum strains isolated from traditional Chinese fermented foods. Food Chem 135: 1914-1919.   DOI
16 Smith TK. 1980. Influence of dietary fiber, protein and zeolite on zearalenone toxicosis in rats and swine. J Anim Sci 50: 278-285.   DOI
17 Sturm G, Jacobs J, Sproer C, Schumann P, Gescher J. 2011. Leucobacter chromiiresistens sp. nov., a chromate-resistant strain. Int J Syst Evol Microbiol 61: 956-960.   DOI
18 Sunar K, Dey P, Chakraborty U, Chakraborty B. 2013. Biocontrol efficacy and plant growth promoting activity of Bacillus altitudinis isolated from Darjeeling hills, India. J Basic Microbiol 55: 91-104.
19 Svec P, Vancanneyt M, Koort J, Naser SM, Hoste B, Vihavainen E, Vandamme P, Swings J, Bjorkroth J. 2005. Enterococcus devriesei sp. nov., associated with animal sources. Int J Syst Evol Microbiol 55: 2479-2484.   DOI
20 Taguchi S, Ozaki A, Momose H. 1998. Engineering of a Cold-Adapted protease by sequential random mutagenesis and a screening system. Appl Environ Microbiol 64: 492-495.
21 Chung TK, Gelberg HB, Dorner JL, Baker DH. 1991. Safety of L-tryptophan for pig. J Anim Sci 69: 2955-2960.   DOI
22 Wenger PN, Tokars JI, Brennan P, Samel C, Bland L, Miller M, Carson L, Arduino M, Edelstein P, Aguero S, Riddle C, O'Hara C, Jarvis W. 1997. An outbreak of Enterobacter hormaechei infection and colonization in an intensive care nursery. Clin Infect Dis 24: 1243-1244.   DOI
23 Widerstrom M, Wistrom J, Ferry S, Karlsson C, Monsen T, 2007. Molecular epidemiology of Staphylococcus saprophyticus isolated from women with uncomplicated community-acquired urinary tract infection. J Clin Microbiol 45: 1561-1564.   DOI
24 Chawanthayatham S, Thiantanawat A, Egner PA, Groopman JD, Wogan GN, Croy RG, Essigmann JM. 2015. Prenatal exposure of mice to the human liver carcinogen aflatoxin B1 reveals a critical window of susceptibility to genetic change. Int J Cancer 136: 1254-1262.   DOI
25 Cheon DS, Chae C. 1996. Outbreak of diarrhea associated with Enterococcus durans in piglets. J Vet Diagn Invest 8: 123-124.   DOI
26 Choi IK, Jung SH, Kim BJ, Park SY, Kim J, Han HU. 2003. Novel Leuconostoc citreum starter culture system for the fermentation of kimchi, a fermented cabbage product. Antonie van Leeuwenhoek, 84: 247-253.   DOI
27 Collins MD, Facklam RR, Farrow JA, Williamson R. 1989. Enterococcus raffinosus sp. nov., Enterococcus solitarius sp. nov. and Enterococcus pseudoavium sp. nov. FEMS microbiol lett 57: 283-288.   DOI
28 Datta S, Holmes B, Park JI, Chen Z, Dibble DC, Hadi M, Blanch HW, Simmons BA, Sapra R. 2010. Ionic liquid tolerant hyperthermophilic cellulases for biomass pretreatment and hydrolysis. Green Chem 12: 338-345.   DOI
29 Blount WP. 1961. Turkey "X" disease. J Brit Turkey Fed 9: 52-77.
30 Lu X, Zhou D, Chen X, Zhang J, Huang H, Wei L. 2017. Isolation and characterization of Bacillus altitudinis JSCX-1 as a new potential biocontrol agent against Phytophthora sojae in soybean [Glycine max (L.) Merr.]. Plant Soil 1-14.
31 Maciorowski KG, Herrera P, Jones FT, Pillai SD, Ricke SC. 2007. Effects on poultry and livestock of feed contamination with bacteria and fungi. Anim Feed Sci Technol 133: 109-136.   DOI
32 Madahaiyan M, Poonguzhali S, Kwon SW, Sa TM. 2010. Bacillus methylotrophicus sp. nov., a methanol-utilizing, plant-growth-promoting bacterium isolated from rice rhizosphere soil. Int J Syst Evol Microbiol 60: 2490-2495.   DOI
33 Mahendran S, Sankaralingam S, Shankar T, Vijayabaskar P. 2010. Alkalophilic protease enzyme production from estuarine Bacillus aquimaris. World J Fish and Marine Sci 2: 436-443.
34 Young JM. 2004. Renaming of Agrobacterium larrymoorei Bouzar and Jones 2001 as Rhizobium larrymoorei (Bouzar and Jones 2001) comb. nov. Int J Syst Evol Microbiol 54: 149.   DOI
35 Tedesco P, Visone M, Parrilli E, Tutino ML, Perrin E, Maida I, Fani R, Ballestriero F, Santos R, Pinilla C, Schiavi ED, Tegos G, De Pascale D. 2015. Investigating the role of the host multidrug resistance associated protein transporter family in Bukholderia cepacia comples pathogenicity using a Caenorhabditis elegans infection model. PLoS ONE 10: e0142883.   DOI
36 Tharvornvee W, Pruksakorn C, Lekcharoensuk P. 2016. Inducible vancomycin resistance is common in porcine Enterococcus gallinarum and E. casseliflavus isolates. Thai J Vet Med 46: 627-635.
37 Thornton VB, Davis JA, St Clair MB, Cole MN. 2003. Inoculation of Staphylococcus xylosus in SJL/J mice to determine pathogenicity. Contemp Top Lab Anim Sci 42: 49-52.
38 Winding A, Santos S, Hendriksen NB, Jakobsen HH. 2015. Fate of pathogenic Bacillus cereus spores after ingestion by protist grazers. Bacterial Genetics and Ecology
39 Yi K, Yeon JS, Kim J, Kim SC, Moon HI, Jeon CO, Lee SS, Kim DW, Kim SK. 2015. Microbiological and chemical changes of complete feed during spoilage. J Life Sci 25: 1148-1155.   DOI
40 Zhang L, Thomas JC, Miragaia M, Bouchami O, Chaves F, d'Azevedo PA, Aanensen DM, de Lencastre H, Gray BM, Robinson DA. 2013. Multilocus sequence typing and further genetic characterization of the enigmatic pathogen, Staphylococcus hominis. PLoS ONE 8: e66496.   DOI
41 Yamanaka T, Sumita-Sasazaki Y, Sugimori C, Matsumoto-Mashimo C, Yamane K, Mizukawa K, Yoshida M, Hayashi H, Nambu T, Leung KP, Fukushima H. 2010. Biofilm-like structures and pathogenicity of Escherichia hermannii YS-11, a clinical isolate from a persistent apical periodontitis lesion. FEMS Immunol Med Microbiol 59: 456-465.   DOI
42 Egamberdieva D, Botir H, Abeer H, Abd-Allah EF. 2014. Characterization of salt tolerant Enterobacter hormaechei strain associated with tomato root grown in arid saline soil. J Pure Appl Microbiol 8: 4231-4239.
43 Doi K, Nishizaki Y, Fujino Y, Ohshima T, Ohmomo S, Ogata S. 2009. Pediococcus lolii sp. nov., isolated from ryegrass silage. Int J Syst Evol Microbiol 59: 1007-1010.   DOI
44 Dunleavy JM. 1989. Curtobacterium plantarum sp. nov. is ubiquitous in plant leaves and is seed transmitted in soybean and corn. Int J Syst Bacteriol 39: 240-249.   DOI
45 Dutkiewicz J, Mackiewicz B, Lemieszek MK, Golec M, Milanowski J. 2016. Pantoea agglomerans: a mysterious bacterium of evil and good. Part III. Deleterious effects: infections of humans, animals and plants. Ann Agric Environ Med 23: 197-205.   DOI
46 Elbanna K, Elnaggar S, Bakeer A. 2014. Characterization of Bacillus altitudinis as a new causative agent of bacterial soft rot. J Phytopathol 162: 712-722.   DOI
47 Fang Y, Lin H, Wu L, Ren D, Ye W, Dong G, Zhu L, Guo L. 2015. Genome sequence of Xanthomonas sacchari R1, a biocontrol bacterium isolated from the rice seed. Genome Announcement 206: 77-78.
48 McCaughey C, Damani NN. 1991. Central venous line infection caused by Brevibacterium epidermidis. J Infect 23: 211-212.   DOI
49 Mahyarudin, Rusmana I, Lestari Y. 2015. Metagenomic of actinomycetes based on 16S rRNA and nifH gene in soil and roots of four Indonesian rice cultivars using PCRDGGE. HAYATI Journal of Biosciences 22: 113-121.   DOI
50 Masoud W, Jakobsen M. 2003. Surface ripened cheeses: the effects of Debaryomyces hansenii, NaCl and pH on the intensity of pigmentation produced by Brevibacterium linens and Corynebacterium flavescens. Int Dairy J 13: 231-237.   DOI
51 Meloche JL, Smith TK. 1995. Altered tissue amino acid metabolism in acute T-2 toxicosis. Proc Soc Exp Biol Med 210: 260-265.   DOI
52 Mishra S, Behera N. 2008. Amylase activity of a starch degrading bacteria isolated from soil receicing kitchen wastes. Afr J Biotechnol 7: 3326-3331.
53 Funke G, Aravena-Roman M, Frodl R. 2005. First description of Curtobacterium spp. isolated from human clinical specimens. J Clin Micobiol 43: 1032-1036.   DOI
54 Fernandes AP, Perl TM, Herwaldt LA. 1996. Staphylococcus cohnii: a case report on an unusual pathogen. Clin Perform Qual Health Care 4: 107-109.
55 Fink-Gremmels J. 2008. The role of mycotoxins in the health and performance of dairy cows. The Veterinary Journal 176: 84-92.   DOI
56 From C, Hormazabal V, Granum PE. 2007. Food poisoning associated with pumilacidin-producing Bacillus pumilus in rice. Int J food microbiol 115: 319-324.   DOI
57 Mrohoshi T, Wang WZ, Someya N, Ikeda T. 2011. Genome sequence of Microbacterium testaceum StLB037, an N-acylhomoserine lactone-degrading bacterium isolated from potato leaves. J Bacteriol 193: 2072-2073.   DOI
58 Moctezuma-Zarate MG, Carvajal-Moreno M, Espinosa-Aguirre JJ, Gonsebatt-Bonaparte ME, Rojo-Callejas F, Castillo-Urueta P, Perez-Lopez I, Ruiz-Velasco S. 2015. Role of pH in the mutagenicity of aflatoxin B1 in maize tortillas during in vitro human digestion model. J Food Nutr Disor 4: 1-10.
59 Morandi S, Silvetti T, Brasca M. 2013. Biotechnological and safety characterization of Enterococcus lactis, a recently described species of dairy origin. Antonie Van Leeuwenhoek 103: 239-249.   DOI
60 Morikawa M. 2006. Beneficial biofilm formation by industrial bacteria Bacillus subtilis and related species. J Biosci Bioeng 101: 1-8.   DOI
61 Hanif NQ, Muhammad G. 2015. Immunotoxicity of ochratoxin A and role of Trichosporon mycotoxinivorans on the humoral response to infectious viral disease vaccines in broilers. Pakistan J Zool 47: 1683-1689.
62 Geider K, Auling G, Du Z, Jakovljevic V, Jock S, Völksch B. 2006. Erwinia tasmaniensis sp. nov., a non-phytopathogenic bacterium from apple and pear trees. Int J Syst Evol Microbiol 56: 2937-2943.   DOI
63 Gillis M, Van Van T, Bardin R, Goor M, Hebbar P, Willems A, Segers P, Kersters K, Heulin T, Fernandez MP. 1995. Polyphasic taxonomy in the genus Burkholderia leading to an emended description of the genus and proposition of Burkholderia vietnamiensis sp. nov. for N2-fixing isolates from rice in Vietnam. Int J Syst Evol Microbiol 45: 274-289.
64 Gomez-Ramirez M, Montero-Alvarez LA, Tobon-Aviles A, Fierros-Romero G, Rojas-Avelizapa NG. 2015. Microbacterium oxydans and Microbacterium liquefaciens: a biological alternative for the treatment of Ni-V-containing wastes. J Environ Sci Health A Tox Hazard Subst Environ Eng 50: 602-610.
65 Hantsis-Zacharov E, Senderovich Y, Halpern M. 2008. Chryseobacterium bovis sp. nov., isolated from raw cow's milk. Int J Syst Evol Microbiol 58: 1024-1028.   DOI
66 Noonin C, Jiravanichpaisal P, Soderhall I, Merino S, Tomas JM, Soderhall K. 2010. Melanization and pathogenicity in the insect, Tenebrio molitor, and the crustacean, Pacifastacus leniusculus, by Aeromonas hydrophila AH-3. PLoS ONE 5: e15728.   DOI
67 Muthukumarasamy R, Cleenwerck I, Revathi G, Vadivelu M, Janssens D, Hoste B, Gum KU, Park KD, Son CY, Sa T, Caballero-Mellado J. 2005. Natural association of Gluconacetobacter diazotrophicus and diazotrophic Acetobacter peroxydans with wetland rice. Syst Appl Microbiol 28: 277-286.   DOI
68 Neef J, Koedijk DG, Bosma T, van Dijl JM, Buist G. 2014. Efficient production of secreted staphylococcal antigens in a non-lysing and proteolytically reduced Lactococcus lactis strain. Appl Microbiol Biotechnol 98: 10131-10141.   DOI
69 Nihorimbere V, Cawoy H, Seyer A, Brunelle A, Thonart P, Ongena M. 2012. Impact of rhizosphere factors on cyclic lipopeptide signature from the plant beneficial strain Bacillus amyloliquefaciens S499. FEMS Microbiol Ecol 79: 176-191.   DOI
70 Bao Y, Zhang Y, Zhang Y, Liu Y, Wang S, Dong X, Wang Y, Zhang H. 2010. Screening of potential probiotic properties of Lactobacillus fermentum isolated from traditional dairy products. Food Control 21: 695-701.   DOI
71 Berg G, Eberl L, Hartmann A. 2005. The rhizosphere as a reservoir for opportunistic human pathogenic bacteria. Environ Microbiol 7: 1673-1685.   DOI
72 Kissell L, Davidson S, Hopkins BA, Smith GW, Whitlow LW. 2012. Effect of experimental feed additives on aflatoxin in milk of dairy cows fed aflatoxin-contaminated diets. J Anim Physiol Anim Nutr 97: 694-700.
73 Hauser E, Kampfer P, Busse HJ. 2004. Pseudomonas psychrotolerans sp. nov. Int J Syst Evol Microbiol 54: 1633-1637.   DOI
74 Hill JE, Baiano JC, Barnes AC. 2009. Isolation of a novel strain of Bacillus pumilus from penaeid shrimp that is inhibitory against marine pathogens. J Fish Dis 32: 1007-1016.   DOI
75 Idriss EE, Makarewicz O, Farouk A, Rosner K, Greiner R, Bochow H, Tichter T, Borriss R. 2002. Extracellular phytase activity of Bacillus amyloliquefaciens FZB45 contributes to its plant-growth-promoting effect. Microbiology 148: 2097-2109.   DOI
76 Pailan S, Gupta D, Apte S, Krishnamurthi S, Saha P. 2015. Degradation of organophosphate insecticide by a novel Bacillus aryabhattai strain SanPS1, isolated from soil of agricultural field in Burdwan, West Bengal, India. Int Biodeterior Biodegrad 103: 191-195.   DOI
77 Pandian SR, Deepak V, Kalishwaralal K, Rameshkumar N, Jeyaraj M, Gurunathan S. 2010. Optimization and fed-batch production of PHB utilizing dairy waste and sea water as nutrient sources by Bacillus megaterium SRKP-3. Bioresour Technol 101: 705-711.   DOI
78 Kang YS, Jung J, Jeon CO, Park W. 2011. Acinetobacter oleivorans sp. nov. is capable of adhering to and growing on diesel-oil. J Microbiol 49: 29-34.   DOI
79 Kim GH, Yi KJ, Lee AR, Jang IH, Song IG, Kim DW, Kim SK. 2014. Viability of probiotics in feed under high temperature conditions and their growth inhibitory effect on contaminant Microbes. Korean J Microbiol 50: 345-350.   DOI
80 Ko KS, Oh WS, Lee MY, Lee JH, Lee H, Peck KR, Lee NY, Song JH. 2006. Bacillus infactis sp. nov. and Bacillus idriensis sp. nov., isolated from a patient with neonatal sepsis. Int J of Sys Evol Microbiol 56: 2541-2544.   DOI
81 Kwak MJ, Jeong H, Madhaiyan M, Lee Y, Sa TM, Oh TK, Kim JF. 2014. Genome information of Methylobacterium oryzae, a plant-probiotic methylotroph in the phyllosphere. PLoS ONE 9: e106704.   DOI
82 Lacey LA. 2007. Bacillus thuringiensis serovariety israelensis and Bacillus sphaericus for mosquito control. J Am Mosq Control Assoc 23: 133-163.   DOI
83 Reva ON, Smimov VV, Pettersson B, Priest FG. 2002. Bacillus endophyticus sp. nov., isolated from the inner tissues of cotton plants (gGossypium sp.). Int J Syst Evol Microbiol 52: 101-107.   DOI
84 Patterson JE, Vecchio J, Pantelick EL, Farrel P, Mazon D, Zervos MJ, Hierholzer WJ Jr. 1991. Association of contaminated gloves with transmission of Acinetobacter calcoaceticus var. anitratus in an intensive care unit. Am J Med 91: 479-483.   DOI
85 Perez C, Pauli M, Bazerque P. 1990. An antibiotic assay by the agar well diffusion method. Acta Biol Med Exp 15: 113-115.
86 Regalado NG, Martin G, Antony SJ. 2009. Acinetobacter lwoffii: bacteremia associated with acute gastroenteritis. Travel Med Infect Dis 7: 316-317.   DOI
87 Rong X, Guo Y, Huang Y. 2009. Proposal to reclassify the Streptomyces albidoflavus clade on the basis of multilocus sequence analysis and DNA-DNA hybridization, and taxonomic elucidation of Streptomyces griseus subsp. solvifaciens. Syst Appl Microbiol 32: 314-322.   DOI
88 Satomi M, La Duc MT, Venkateswaran K. 2006. Bacillus safensis sp. nov., isolated from spacecraft and assembly-facility surfaces. Int J Syst Evol Microbiol 56: 1735-1740.   DOI