Isolation, Identification and Biological Characteristics Analysis of Citrobacter freundii from Cynomolgus Monkey (Macaca fascicularis)

doi:10.12300/j.issn.1674-5817.2025.150

Abstract

Abstract:

Objective Identification and analysis, animal regression test, and drug susceptibility study were conducted on a pathogenic strain causing diarrhea in cynomolgus monkeys, aiming to provide a practical basis for the clinical treatment of Citrobacter freundii. Methods Fresh fecal samples were collected from nine diarrheal cynomolgus monkeys and streaked on Salmonella-Shigella (SS) medium, LB medium, and Columbia blood agar medium, and incubated at 37 ℃ for 24 h. Subsequently, the isolated strain was identified by colony morphology observation, Gram staining, biochemical tests and 16S rRNA gene sequencing, and PCR was used to detect its major virulence genes. After propagation, the isolate was intragastrically administered to healthy cynomolgus monkeys and C57BL/6 mice for animal regression tests to evaluate its pathogenicity. Finally, the disk-diffusion method was used to detect the antimicrobial susceptibility of the isolate. Results A single bacterial strain, designated MF071743, was isolated from 9 fecal samples collected from diarrheal cynomolgus monkeys. The isolate formed pink, smooth, round colonies on SS medium; translucent, smooth, moist, shiny colonies with neat edges on LB medium; and smooth, moist, off-white colonies on Columbia blood agar medium. Gram staining revealed that the isolate was a Gram-negative, spore-free short bacillus. Biochemical tests showed that the isolate was positive for motility test, mannitol test, hydrogen sulfide test, methyl red test, citrate utilization test, gas production from glucose test, raffinose test, sorbitol test, and D-xylose test, but negative for phenylalanine test, gluconate test, indole test, Voges Proskauer (VP) test, urease test, lysine test, ornithine test, and adonitol test. The results of 16S rRNA gene sequencing showed that the gene sequence similarity between strain MF071743 and Citrobacter freundii was 99.0%. PCR results showed that this strain carries genes encoding the urease accessory proteins UreD, UreE, and UreF. Animal intragastric administration assays demonstrated that the strain caused loose stools in cynomolgus monkeys, and all C57BL/6 mice died within 72 h. Drug susceptibility test results indicated that the isolate was sensitive to 16 antibiotics, including ceftriaxone, amikacin, gentamicin, ceftazidime, and levofloxacin, while it exhibited resistance to 5 antibiotics, including ampicillin, cefazolin, vancomycin, erythromycin, and cephalexin. Conclusion A strain of Citrobacter freundii with certain drug resistance was isolated from the feces of diarrheal cynomolgus monkeys. The results of this study provide a reference for the diagnosis and treatment of gastrointestinal diseases in captive laboratory monkeys.

Key words: Cynomolgus monkey, Citrobacter freundii, Bacterial culture, Isolation and identification, Phylogenetic analysis

CLC Number:

S852.61
S858

LI Heling,QIAN Ziyao,QIN Gangmin,et al. Isolation, Identification and Biological Characteristics Analysis of Citrobacter freundii from Cynomolgus Monkey (Macaca fascicularis)[J]. Laboratory Animal and Comparative Medicine, 2026, 46(3): 367-377. DOI: 10.12300/j.issn.1674-5817.2025.150.

Figures/Tables 7

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引物名称 Primer name	引物序列(5'→3') Primer sequence (5'→3')		退火温度/℃ Annealing temperature/℃	预期长度/bp Expected length/bp
16S rRNA	F: AGAGTTTGATCCTGGCTCAG	R: CGGTTACCTTGTTACGACTT	55.0	1 500
cfa	F: TCCAGCGCATTCA	R: TCCAGCCTTCGGCAAACG	60.5	100
ureABC	F: ATGGAACTGACTCCCAGAG	R: TCAAAACAGAAAATAGCGTTGCGCC	56.5	2 328
ureD	F: CCGCAAGAGGACGTTTGC	R: CCGACCCAGGGATGATGT	60.0	459
ureE	F: ACCCAACGCCTTGACCAC	R: AGGATTTGCAGCGGAACG	63.7	293
ureF	F: TGGAAATCGGCTGGGTGA	R: CCCGACTGCGTTCTTCATC	65.0	210
ureG	F: ATCAGCGCATTCTCACCG	R: CAATAATCGTCGCCAGACC	53.2	438

引物名称 Primer name	引物序列(5'→3') Primer sequence (5'→3')		退火温度/℃ Annealing temperature/℃	预期长度/bp Expected length/bp
16S rRNA	F: AGAGTTTGATCCTGGCTCAG	R: CGGTTACCTTGTTACGACTT	55.0	1 500
cfa	F: TCCAGCGCATTCA	R: TCCAGCCTTCGGCAAACG	60.5	100
ureABC	F: ATGGAACTGACTCCCAGAG	R: TCAAAACAGAAAATAGCGTTGCGCC	56.5	2 328
ureD	F: CCGCAAGAGGACGTTTGC	R: CCGACCCAGGGATGATGT	60.0	459
ureE	F: ACCCAACGCCTTGACCAC	R: AGGATTTGCAGCGGAACG	63.7	293
ureF	F: TGGAAATCGGCTGGGTGA	R: CCCGACTGCGTTCTTCATC	65.0	210
ureG	F: ATCAGCGCATTCTCACCG	R: CAATAATCGTCGCCAGACC	53.2	438

检测项目 Test items	结果 Results	标准菌株 Reference strains
甘露醇试验 Mannitol test	+	+
硫化氢试验 H₂S test	+	±
苯丙氨酸试验 Phenylalanine test	-	-
葡萄糖酸盐试验 Gluconate test	-	-
吲哚试验 Indigo test	-	±
VP试验 Voges Proskauer test	-	-
甲基红试验 Methyl red test	+	+
枸橼酸盐试验 Citrate test	+	±
脲酶试验 Urease test	-	±
葡萄糖产气试验 Glucose gas production test	+	±
赖氨酸试验 Lysine test	-	-
鸟氨酸试验 Ornithine test	-	±
棉子糖试验 Raffinose test	+	±
山梨醇试验 Sorbitol test	+	±
侧金盏花醇试验 Adonitol test	-	-
木糖试验 Xylose test	+	±

检测项目 Test items	结果 Results	标准菌株 Reference strains
甘露醇试验 Mannitol test	+	+
硫化氢试验 H₂S test	+	±
苯丙氨酸试验 Phenylalanine test	-	-
葡萄糖酸盐试验 Gluconate test	-	-
吲哚试验 Indigo test	-	±
VP试验 Voges Proskauer test	-	-
甲基红试验 Methyl red test	+	+
枸橼酸盐试验 Citrate test	+	±
脲酶试验 Urease test	-	±
葡萄糖产气试验 Glucose gas production test	+	±
赖氨酸试验 Lysine test	-	-
鸟氨酸试验 Ornithine test	-	±
棉子糖试验 Raffinose test	+	±
山梨醇试验 Sorbitol test	+	±
侧金盏花醇试验 Adonitol test	-	-
木糖试验 Xylose test	+	±

药物 Drug	药物含量/（µg·片^-1) Drug dose /(µg·disc^-1)	抑菌圈直径/mm Inhibition zone diameter/mm	判定结果 Assessment result	判定标准/mm Judgement standard/mm
药物 Drug	药物含量/（µg·片^-1) Drug dose /(µg·disc^-1)	抑菌圈直径/mm Inhibition zone diameter/mm	判定结果 Assessment result	R	I	S
头孢曲松 Ceftriaxone	30	30	S	≤13	14～22	≥23
阿米卡星 Amikacin	30	24	S	≤14	15～16	≥17
庆大霉素 Gentamicin	10±2.5	19	S	≤12	13～14	≥15
氨苄西林 Ampicillin	10	10	R	≤13	14～16	≥17
头孢唑啉 Cefazolin	30	7	R	≤14	15～17	≥18
头孢他啶 Ceftazidime	30	26	S	≤17	18～20	≥21
左氧氟沙星 Levofloxacin	5	28	S	≤13	14～16	≥17
万古霉素 Vancomycin	30	7	R	≤9	10～11	≥12
复方磺胺甲��唑 Co-trimoxazole	23.75	24	S	≤10	11～15	≥16
环丙沙星 Ciprofloxacin	5	29	S	≤15	16～20	≥21
诺氟沙星 Norfloxacin	10	27	S	≤12	13～16	≥17
红霉素 Erythromycin	15	7	R	≤13	14～22	≥23
利福平 Rifampicin	5	7	I	≤6	7～9	≥10
阿莫西林 Amoxicillin	10	10	S	≤5	6～9	≥10
呋喃唑酮 Furazolidone	300	18	S	≤5	6～9	≥10
林可霉素 Lincomycin	2	7	I	≤5	6～11	≥12
多黏菌素B Polymyxin B	300	13	S	≤8	9～11	≥12
头孢哌酮 Cefoperazone	75	31	S	≤15	16～20	≥21
头孢氨苄 Cephalexin	30	7	R	≤13	14～16	≥17
氧氟沙星 Ofloxacin	5	28	S	≤12	13～15	≥16
杆菌肽 Bacitracin	0.04	7	I	≤6	7～9	≥10
亚胺培南 Imipenem	10	23	S	≤19	20～22	≥23
美罗培南 Meropenem	10	28	S	≤19	20～22	≥23
阿奇霉素 Azithromycin	15	18	S	≤12	–	≥13