生物被膜在动物细菌感染致病机理中的作用

doi:10.11843/j.issn.0366-6964.2025.01.010

摘要/Abstract

摘要：

细菌的生物被膜是指菌体嵌入自身产生的保护性基质中所形成的细菌聚集体。基于生物被膜的生存方式有助于微生物抵御机体的免疫反应和药物作用等外部威胁，因此，细菌的生物被膜会加重感染，并导致严重的动物疾病。生物被膜在动物病原菌的致病机理中发挥着诱导、调节局部炎症反应和促进细胞内侵袭等作用，其物理屏障作用可为病原体提供保护，影响治疗效果，并增加慢性感染和亚临床感染的风险。饲养动物、野生动物和伴侣动物等均可被细菌及其生物被膜感染，文章综述了细菌生物被膜在动物心血管、中枢神经、消化、生殖、呼吸、泌尿和皮肤等系统感染致病机理中的作用，以期为细菌生物被膜感染的准确检测和有效治疗提供参考。

关键词: 生物被膜, 细菌, 动物, 慢性感染

Abstract:

Bacteria biofilm refers to the bacterial aggregates formed by embedding the bacterial into the protective matrix which self produces. The survival mode based on biofilms helps microorganisms resist external threats such as immune system and drug treatments. Therefore, biofilms of bacterial organisms can exacerbate bacterial infections and lead to serious animal diseases. Biofilm plays a role in the pathogenesis of animal pathogens, including inducing and regulating local inflammatory responses and promoting intracellular invasion. The physical barrier function can provide protection for pathogens, reduce the treatment effectiveness, and increase the risk of chronic and subclinical infections. Bacteria and their biofilms can infect husbandry animals, wild animals, and companion animals. The review shows the role of biofilms in the pathogenesis of bacterial infections in animal cardiovascular, central nervous, digestive, reproductive, respiratory, urinary, and skin systems, aiming to provide reference for accurate detection and effective treatment of animal bacterial biofilms.

Key words: biofilm, bacterial, animals, chronic infection

中图分类号:

S852.61

张蕾, 陈亮, 冯万宇, 兰世捷, 苗艳, 田秋丰, 白长胜, 张备, 董佳强, 江波涛, 王洪宝, 史同瑞, 黄宣凯. 生物被膜在动物细菌感染致病机理中的作用[J]. 畜牧兽医学报, 2025, 56(1): 107-114.

ZHANG Lei, CHEN Liang, FENG Wanyu, LAN Shijie, MIAO Yan, TIAN Qiufeng, BAI Changsheng, ZHANG Bei, DONG Jiaqiang, JIANG Botao, WANG Hongbao, SHI Tongrui, HUANG Xuankai. The Role of Biofilms in the Pathogenesis of Animal Bacterial Infections[J]. Acta Veterinaria et Zootechnica Sinica, 2025, 56(1): 107-114.

参考文献 57

1	HØIBY N . A short history of microbial biofilms and biofilm infections[J]. Apmis, 2017, 125 (4): 272- 275. doi: 10.1111/apm.12686
2	VESTBY L K , GRØNSETH T , SIMM R , et al. Bacterial biofilm and its role in the pathogenesis of disease[J]. Antibiotics (Basel), 2020, 9 (2): 59. doi: 10.3390/antibiotics9020059
3	ANJU V T , BUSI S , IMCHEN M , et al. Polymicrobial infections and biofilms: clinical significance and eradication strategies[J]. Antibiotics (Basel), 2022, 11 (12): 1731. doi: 10.3390/antibiotics11121731
4	TOLKER-NIELSEN T. Biofilm development[M] //GHANNOUM M, PARSEK M, WHITELEY M, et al. Microbial Biofilms. 2nd ed. Washington: ASM Press, 2015: 51-66.
5	SOLANO C , ECHEVERZ M , LASA I . Biofilm dispersion and quorum sensing[J]. Curr Opin Microbiol, 2014, 18, 96- 104. doi: 10.1016/j.mib.2014.02.008
6	RYBTKE M , HULTQVIST L D , GIVSKOV M , et al. Pseudomonas aeruginosa biofilm infections: community structure, antimicrobial tolerance and immune response[J]. J Mol Biol, 2015, 427 (23): 3628- 3645. doi: 10.1016/j.jmb.2015.08.016
7	YANG S S , LI X F , CANG W H , et al. Biofilm tolerance, resistance and infections increasing threat of public health[J]. Microb Cell, 2023, 10 (11): 233- 247. doi: 10.15698/mic2023.11.807
8	ZHAO A L , SUN J Z , LIU Y P . Understanding bacterial biofilms: from definition to treatment strategies[J]. Front Cell Infect Microbiol, 2023, 13, 1137947. doi: 10.3389/fcimb.2023.1137947
9	O'TOOLE D , ALLEN T , HUNTER R , et al. Diagnostic exercise: myocarditis due to Histophilus somni in feedlot and backgrounded cattle[J]. Vet Pathol, 2009, 46 (5): 1015- 1017. doi: 10.1354/vp.08-VP-0332-O-DEX
10	DE YANIZ M G , FIORENTINO M A , GARCÍA J P , et al. Clinical-pathological findings induced by Histophilus somni isolated in subacute cardiac death in feedlot cattle[J]. Vet Res Commun, 2023, 47 (2): 683- 691. doi: 10.1007/s11259-022-10028-3
11	SANDAL I , SHAO J Q , ANNADATA S , et al. Histophilus somni biofilm formation in cardiopulmonary tissue of the bovine host following respiratory challenge[J]. Microbes Infect, 2009, 11 (2): 254- 263. doi: 10.1016/j.micinf.2008.11.011
12	ELSWAIFI S F , SCARRATT W K , INZANA T J . The role of lipooligosaccharide phosphorylcholine in colonization and pathogenesis of Histophilus somni in cattle[J]. Vet Res, 2012, 43 (1): 49. doi: 10.1186/1297-9716-43-49
13	RAABE V N, SHANE A L. Group B Streptococcus (Streptococcus agalactiae)[J/OL]. Microbiol Spectr, 2019, 7(2): 10.1128/microbiolspec.gpp3-0007-2018. [2023-03-21]. https://journals.asm.org/doi/epub/10.1128/microbiolspec.gpp3-0007-2018.
14	PHUOC N N , LINH N T H , CRESTANI C , et al. Effect of strain and enviromental conditions on the virulence of Streptococcus agalactiae (Group B Streptococcus; GBS) in red tilapia (Oreochromis sp.)[J]. Aquaculture, 2021, 534, 736256. doi: 10.1016/j.aquaculture.2020.736256
15	ISIAKU A I , SABRI M Y , INA-SALWANY M Y , et al. Biofilm is associated with chronic streptococcal meningoencephalitis in fish[J]. Microb Pathog, 2017, 102, 59- 68. doi: 10.1016/j.micpath.2016.10.029
16	PATRAS K A , DERIEUX J , AL-BASSAM M M , et al. Group B Streptococcus biofilm regulatory protein A contributes to bacterial physiology and innate immune resistance[J]. J Infect Dis, 2018, 218 (10): 1641- 1652. doi: 10.1093/infdis/jiy341
17	MOTTA J P , WALLACE J L , BURET A G , et al. Gastrointestinal biofilms in health and disease[J]. Nat Rev Gastroenterol Hepatol, 2021, 18 (5): 314- 334. doi: 10.1038/s41575-020-00397-y
18	HATHROUBI S , SERVETAS S L , WINDHAM I , et al. Helicobacter pylori biofilm formation and its potential role in pathogenesis[J]. Microbiol Mol Biol Rev, 2018, 82 (2): e00001- 18.
19	MILLER A L , PASTERNAK J A , MEDEIROS N J , et al. In vivo synthesis of bacterial amyloid curli contributes to joint inflammation during S. Typhimurium infection[J]. PLoS Pathog, 2020, 16 (7): e1008591. doi: 10.1371/journal.ppat.1008591
20	PETRUZZI B L. Pasteurella multocida biofilm formation, and the interrelationship of P. multocida with Histophilus somni in a polymicrobial biofilm during bovine respiratory disease[D]. Blacksburg: Virginia Tech, 2018.
21	TAJIMA M , YAGIHASHI T . Interaction of Mycoplasma hyopneumoniae with the porcine respiratory epithelium as observed by electron microscopy[J]. Infect Immun, 1982, 37 (3): 1162- 1169. doi: 10.1128/iai.37.3.1162-1169.1982
22	TONNI M , FORMENTI N , BONIOTTI M B , et al. The role of co-infections in M. hyopneumoniae outbreaks among heavy fattening pigs: a field study[J]. Vet Res, 2022, 53 (1): 41. doi: 10.1186/s13567-022-01061-w
23	RAYMOND B B A , JENKINS C , TURNBULL L , et al. Extracellular DNA release from the genome-reduced pathogen Mycoplasma hyopneumoniae is essential for biofilm formation on abiotic surfaces[J]. Sci Rep, 2018, 8 (1): 10373. doi: 10.1038/s41598-018-28678-2
24	WU Y Z , YU Y F , HUA L Z , et al. Genotyping and biofilm formation of Mycoplasma hyopneumoniae and their association with virulence[J]. Vet Res, 2022, 53 (1): 95. doi: 10.1186/s13567-022-01109-x
25	TREMBLAY Y D N , LABRIE J , CHÉNIER S , et al. Actinobacillus pleuropneumoniae grows as aggregates in the lung of pigs: is it time to refine our in vitro biofilm assays?[J]. Microb Biotechnol, 2017, 10 (4): 756- 760. doi: 10.1111/1751-7915.12432
26	HATHROUBI S , LOERA-MURO A , GUERRERO-BARRERA A L , et al. Actinobacillus pleuropneumoniae biofilms: role in pathogenicity and potential impact for vaccination development[J]. Anim Health Res Rev, 2018, 19 (1): 17- 30. doi: 10.1017/S146625231700010X
27	SLOAN G P , LOVE C F , SUKUMAR N , et al. The Bordetella Bps polysaccharide is critical for biofilm development in the mouse respiratory tract[J]. J Bacteriol, 2007, 189 (22): 8270- 8276. doi: 10.1128/JB.00785-07
28	FULLEN A R , GUTIERREZ-FERMAN J L , RAYNER R E , et al. Architecture and matrix assembly determinants of Bordetella pertussis biofilms on primary human airway epithelium[J]. PLoS Pathog, 2023, 19 (2): e1011193. doi: 10.1371/journal.ppat.1011193
29	WANG M L , LIU M C , XU J , et al. Uterine microbiota of dairy cows with clinical and subclinical endometritis[J]. Front Microbiol, 2018, 9, 2691. doi: 10.3389/fmicb.2018.02691
30	AHMADI M R , DERAKHSHANDEH A , SHIRIAN S , et al. Detection of bacterial biofilm in uterine of repeat breeder dairy cows[J]. Asian Pac J Reprod, 2017, 6 (3): 136- 139. doi: 10.12980/apjr.6.20170308
31	RZEWUSKA M , KWIECIEŃ E , CHROBAK-CHMIEL D , et al. Pathogenicity and virulence of Trueperella pyogenes: a review[J]. Int J Mol Sci, 2019, 20 (11): 2737. doi: 10.3390/ijms20112737
32	LIU M C , WANG B , LIANG H M , et al. Determination of the expression of three fimbrial subunit proteins in cultured Trueperella pyogenes[J]. Acta Vet Scand, 2018, 60 (1): 53. doi: 10.1186/s13028-018-0407-3
33	FERRIS R A , MCCUE P M , BORLEE G I , et al. Model of chronic equine endometritis involving a Pseudomonas aeruginosa biofilm[J]. Infect Immun, 2017, 85 (12): e00332- 17.
34	李琴, 周静茹, 张旭华, 等. 铜绿假单胞菌鞭毛基因fliI的敲除对其鞭毛形成及生物膜生成的影响[J]. 中国人兽共患病学报, 2023, 39 (9): 837- 842.
	LI Q , ZHOU J R , ZHANG X H , et al. Influence of Pseudomonas aeruginosa fliI gene deletion on flagellar and biofilm formation[J]. Chinese Journal of Zoonoses, 2023, 39 (9): 837- 842.
35	TUON F F , DANTAS L R , SUSS P H , et al. Pathogenesis of the Pseudomonas aeruginosa biofilm: a review[J]. Pathogens, 2022, 11 (3): 300. doi: 10.3390/pathogens11030300
36	HENSEN S M , PAVIČIĆ M , LOHUIS J , et al. Location of Staphylococcus aureus within the experimentally infected bovine udder and the expression of capsular polysaccharide type 5 in situ[J]. J Dairy Sci, 2000, 83 (9): 1966- 1975. doi: 10.3168/jds.S0022-0302(00)75073-9
37	SCHÖNBORN S , KRÖMKER V . Detection of the biofilm component polysaccharide intercellular adhesin in Staphylococcus aureus infected cow udders[J]. Vet Microbiol, 2016, 196, 126- 128. doi: 10.1016/j.vetmic.2016.10.023
38	CHEUNG G Y C , BAE J S , OTTO M . Pathogenicity and virulence of Staphylococcus aureus[J]. Virulence, 2021, 12 (1): 547- 569. doi: 10.1080/21505594.2021.1878688
39	PÉREZ M M , PRENAFETA A , VALLE J , et al. Protection from Staphylococcus aureus mastitis associated with poly-N-acetyl β-1, 6 glucosamine specific antibody production using biofilm-embedded bacteria[J]. Vaccine, 2009, 27 (17): 2379- 2386. doi: 10.1016/j.vaccine.2009.02.005
40	SALINA A , GUIMARÃES F F , PEREIRA V B R , et al. Detection of icaA, icaD, and bap genes and biofilm production in Staphylococcus aureus and non-aureus staphylococci isolated from subclinical and clinical bovine mastitis[J]. Arq Bras Med Vet Zootec, 2020, 72 (3): 1034- 1038. doi: 10.1590/1678-4162-11284
41	ZUNIGA E , MELVILLE P A , SAIDENBERG A B S , et al. Occurrence of genes coding for MSCRAMM and biofilm-associated protein Bap in Staphylococcus spp. isolated from bovine subclinical mastitis and relationship with somatic cell counts[J]. Microb Pathog, 2015, 89, 1- 6. doi: 10.1016/j.micpath.2015.08.014
42	朱妍, 刘慧燕, 闫丹丽, 等. 益生菌缓解金黄色葡萄球菌感染牛乳腺炎的研究与应用进展[J]. 中国乳品工业, 2024, 52 (1): 33- 39.
	ZHU Y , LIU H Y , YAN D L , et al. Research status of probiotics in alleviating bovine mastitis caused by Staphylococcus aureus[J]. China Dairy Industry, 2024, 52 (1): 33- 39.
43	GRUNERT T , STESSL B , WOLF F , et al. Distinct phenotypic traits of Staphylococcus aureus are associated with persistent, contagious bovine intramammary infections[J]. Sci Rep, 2018, 8 (1): 15968. doi: 10.1038/s41598-018-34371-1
44	BORTOLAMI A , ZENDRI F , MACIUCA E I , et al. Diversity, virulence, and clinical significance of extended-spectrum β-lactamase-and pAmpC-producing Escherichia coli from companion animals[J]. Front Microbiol, 2019, 10, 1260. doi: 10.3389/fmicb.2019.01260
45	CLARK H , LASAREV M , WOOD M . Risk factors of enterococcal bacteriuria in cats: a retrospective study[J]. Can Vet J, 2023, 64 (1): 40- 44.
46	BALLASH G A , MOLLENKOPF D F , DIAZ-CAMPOS D , et al. Pathogenomics and clinical recurrence influence biofilm capacity of Escherichia coli isolated from canine urinary tract infections[J]. PLoS One, 2022, 17 (8): e0270461. doi: 10.1371/journal.pone.0270461
47	DORSCH R , TEICHMANN-KNORRN S , SJETNE LUND H . Urinary tract infection and subclinical bacteriuria in cats: a clinical update[J]. J Feline Med Surg, 2019, 21 (11): 1023- 1038. doi: 10.1177/1098612X19880435
48	BALDIRIS-AVILA R , MONTES-ROBLEDO A , BUELVAS-MONTES Y . Phylogenetic classification, biofilm-forming capacity, virulence factors, and antimicrobial resistance in uropathogenic Escherichia coli (UPEC)[J]. Curr Microbiol, 2020, 77 (11): 3361- 3370. doi: 10.1007/s00284-020-02173-2
49	杨阳, 吴建国, 肖天兵, 等. 尿路感染的持续复发与多菌感染的研究进展[J]. 国外医药(抗生素分册), 2023, 44 (6): 373- 378. doi: 10.3969/j.issn.1001-8751.2023.06.003
	YANG Y , WU J G , XIAO T B , et al. Advances in the study of persistent recurrence of urinary tract infection with polymicrobial infection[J]. World Notes on Antibiotics, 2023, 44 (6): 373- 378. doi: 10.3969/j.issn.1001-8751.2023.06.003
50	JØRGENSEN E , BJARNSHOLT T , JACOBSEN S . Biofilm and equine limb wounds[J]. Animals (Basel), 2021, 11 (10): 2825.
51	WESTGATE S J , PERCIVAL S L , KNOTTENBELT D C , et al. Microbiology of equine wounds and evidence of bacterial biofilms[J]. Vet Microbiol, 2011, 150 (1-2): 152- 159. doi: 10.1016/j.vetmic.2011.01.003
52	JØRGENSEN E , BAY L , BJARNSHOLT T , et al. The occurrence of biofilm in an equine experimental wound model of healing by secondary intention[J]. Vet Microbiol, 2017, 204, 90- 95. doi: 10.1016/j.vetmic.2017.03.011
53	KÖNIG L M , KLOPFLEISCH R , HÖPER D , et al. Next generation sequencing analysis of biofilms from three dogs with postoperative surgical site infection[J]. Int Sch Res Notices, 2014, 2014, 282971.
54	THAARUP I C , IVERSEN A K S , LICHTENBERG M , et al. Biofilm survival strategies in chronic wounds[J]. Microorganisms, 2022, 10 (4): 775. doi: 10.3390/microorganisms10040775
55	WATTERS C , DELEON K , TRIVEDI U , et al. Pseudomonas aeruginosa biofilms perturb wound resolution and antibiotic tolerance in diabetic mice[J]. Med Microbiol Immunol, 2013, 202 (2): 131- 141. doi: 10.1007/s00430-012-0277-7
56	METCALF D G , BOWLER P G . Biofilm delays wound healing: a review of the evidence[J]. Burns Trauma, 2013, 1 (1): 5- 12. doi: 10.4103/2321-3868.113329
57	PASTAR I , NUSBAUM A G , GIL J , et al. Interactions of methicillin resistant Staphylococcus aureus USA300 and Pseudomonas aeruginosa in polymicrobial wound infection[J]. PLoS One, 2013, 8 (2): e56846. doi: 10.1371/journal.pone.0056846

[1]	吕永乐, 郑雯, 王签慧, 朱家琦, 黄晓琦, 曹中赞, 栾新红. 抗代谢相关脂肪性肝病的天然活性物质研究进展[J]. 畜牧兽医学报, 2025, 56(1): 45-62.
[2]	孙同玉, 马涛. 反刍动物初乳microRNA组成和功能研究进展[J]. 畜牧兽医学报, 2025, 56(1): 74-81.
[3]	章琦, 郭江鹏, 倪爱心, 杜洪峰, 陈继兰, 孙研研. 蛋鸡啄羽行为的影响因素与遗传调控基础研究进展[J]. 畜牧兽医学报, 2024, 55(9): 3745-3756.
[4]	张肖旭, 李昊, 冯平捷, 杨豪, 李新月, 吕冉, 潘章源, 储明星. 单细胞转录组测序技术在家养动物中的应用[J]. 畜牧兽医学报, 2024, 55(8): 3276-3287.
[5]	崔恒洁, 覃金珑, 朱志豪, 鲍雪, 栗绍文, 孟宪荣. 金黄色葡萄球菌对苯扎溴铵敏感性与生物被膜形成能力相关性分析[J]. 畜牧兽医学报, 2024, 55(8): 3669-3677.
[6]	陈秀琴, 林甦, 张世忠, 郑敏, 黄梅清. 基于CRISPR/Cas系统的生物传感器在动物疫病诊断中的应用[J]. 畜牧兽医学报, 2024, 55(7): 2859-2876.
[7]	郑焕琴, 姜晓敏, 岳红, 王宝岩, 刘洋, 张兴晓, 张建龙, 朱洪伟. 猫1型疱疹病毒分离鉴定及部分生物学特性分析[J]. 畜牧兽医学报, 2024, 55(7): 3040-3048.
[8]	季小禹, 王永伟, 邱妍, 张才. 甘草多糖的生理功能及其在畜禽生产中的应用[J]. 畜牧兽医学报, 2024, 55(6): 2379-2387.
[9]	张元旭, 李竟, 王泽昭, 陈燕, 徐凌洋, 张路培, 高雪, 高会江, 李俊雅, 朱波, 郭鹏. 动物遗传评估软件研究进展[J]. 畜牧兽医学报, 2024, 55(5): 1827-1841.
[10]	张吉贤, 范定坤, 付域泽, 焦帅, 马涛, 毕研亮, 张乃锋. 后生素调控动物肠道健康的作用机制及应用进展[J]. 畜牧兽医学报, 2024, 55(5): 1926-1935.
[11]	邓梏男, 张家祺, 保志鹏, 陈涛云, 喻琦胜, 丁露, 朱晨曦, 王怡, 任玉鹏, 贺超, 张斌. 猫疱疹病毒1型的检测及一株分离毒株的致病性[J]. 畜牧兽医学报, 2024, 55(5): 2253-2258.
[12]	黄杰, 阮子豪, 蔡瑞. 抗菌肽在猪精液常温保存中的应用研究进展[J]. 畜牧兽医学报, 2024, 55(4): 1401-1411.
[13]	刘思弟, 马贲, 郑言, 邱云桥, 姚泽龙, 曹中赞, 栾新红. 肠道菌群调控动物肠道黏膜免疫和炎症的研究进展[J]. 畜牧兽医学报, 2024, 55(4): 1423-1431.
[14]	李菲菲, 张晨淼, 童津津, 蒋林树. 线粒体自噬调节NLRP3炎症小体活性改善动物健康的作用机制[J]. 畜牧兽医学报, 2024, 55(4): 1446-1455.
[15]	李钰浚, 何翃闳, 杨丽雪, 杨小耿, 李键, 张慧珠. 线粒体自噬调控哺乳动物胚胎发育的研究进展[J]. 畜牧兽医学报, 2024, 55(3): 905-912.