Jing Liu, Jiaqing Guo, Melanie A Whitmore, Isabel Tobin, Dohyung M Kim, Zijun Zhao, Guolong Zhang
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Although no notable changes were observed at 3 dpi, significant alterations of the microbiota occurred in both the ileum and cecum at 5 and 7 dpi. By 14 dpi, the intestinal microbiota tended to return to a healthy state. Notably, <i>Lactobacillus</i> was enriched in response to <i>E. maxima</i> infection in both the ileum and cecum, although individual <i>Lactobacillus</i>, <i>Ligilactobacillus</i>, and <i>Limosilactobacillus</i> species varied in the temporal pattern of response. Concurrently, major short-chain fatty acid-producing bacteria, such as <i>Faecalibacterium</i>, were progressively suppressed by <i>E. maxima</i> in the cecum. On the other hand, opportunistic pathogens such as <i>Escherichia</i>, <i>Enterococcus</i>, and <i>Staphylococcus</i> were significantly enriched in the ileum during acute infection.</p><p><strong>Importance: </strong>We have observed for the first time the dynamic response of the intestinal microbiota to <i>Eimeria maxima</i> infection, synchronized with its life cycle. Minimal changes occur in both the ileal and cecal microbiota during early infection, while significant alterations coincide with acute infection and disruption of the intestinal mucosal lining. As animals recover from coccidiosis, the intestinal microbiota largely returns to normal. <i>E. maxima</i>-induced intestinal inflammation likely creates an environment conducive to the growth of aerotolerant anaerobes such as <i>Lactobacillus</i>, as well as facultative anaerobes such as <i>Escherichia</i>, <i>Enterococcus</i>, and <i>Staphylococcus</i>, while suppressing the growth of obligate anaerobes such as short-chain fatty acid-producing bacteria. These findings expand our understanding of the temporal dynamics of the microbiota structure during <i>Eimeria</i> infection and offer insights into the pathogenesis of coccidiosis, supporting the rationale for microbiome-based strategies in the control and prevention of this condition.</p>","PeriodicalId":18670,"journal":{"name":"Microbiology spectrum","volume":null,"pages":null},"PeriodicalIF":3.7000,"publicationDate":"2024-10-03","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11448223/pdf/","citationCount":"0","resultStr":"{\"title\":\"Dynamic response of the intestinal microbiome to <i>Eimeria maxima-</i>induced coccidiosis in chickens.\",\"authors\":\"Jing Liu, Jiaqing Guo, Melanie A Whitmore, Isabel Tobin, Dohyung M Kim, Zijun Zhao, Guolong Zhang\",\"doi\":\"10.1128/spectrum.00823-24\",\"DOIUrl\":null,\"url\":null,\"abstract\":\"<p><p><i>Eimeria maxima</i> is a major cause of coccidiosis in chickens and a key predisposing factor for other economically significant diseases such as necrotic enteritis. However, a detailed understanding of the intestinal microbiome response to <i>E. maxima</i> infection is still lacking. This study aimed to comprehensively investigate the dynamic changes of the intestinal microbiome for 14 days post-infection (dpi) with <i>E. maxima</i>. Bacterial 16S rRNA gene sequencing was performed with the ileal and cecal digesta collected from mock and <i>E. maxima-</i>infected chickens at the prepatent (3 dpi), acute (5 and 7 dpi), and recovery phases (10 and 14 dpi) of infection. Although no notable changes were observed at 3 dpi, significant alterations of the microbiota occurred in both the ileum and cecum at 5 and 7 dpi. By 14 dpi, the intestinal microbiota tended to return to a healthy state. Notably, <i>Lactobacillus</i> was enriched in response to <i>E. maxima</i> infection in both the ileum and cecum, although individual <i>Lactobacillus</i>, <i>Ligilactobacillus</i>, and <i>Limosilactobacillus</i> species varied in the temporal pattern of response. 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引用次数: 0
摘要
Eimeria maxima 是鸡球虫病的主要病因,也是坏死性肠炎等其他经济意义疾病的主要诱发因素。然而,目前仍缺乏对 E. maxima 感染后肠道微生物组反应的详细了解。本研究旨在全面调查感染 E. maxima 后 14 天(dpi)肠道微生物组的动态变化。在感染前(3 dpi)、急性期(5 dpi 和 7 dpi)和恢复期(10 dpi 和 14 dpi),对模拟鸡和感染了 E. maxima 的鸡的回肠和盲肠消化物进行了细菌 16S rRNA 基因测序。虽然在 3 dpi 没有观察到明显的变化,但在 5 和 7 dpi 回肠和盲肠的微生物群发生了显著变化。到 14 dpi 时,肠道微生物群趋于恢复到健康状态。值得注意的是,回肠和盲肠中的乳酸杆菌对E. maxima感染都有富集作用,尽管单个乳酸杆菌、ligilactobacillus和Limosilactobacillus物种在反应的时间模式上有所不同。与此同时,产生短链脂肪酸的主要细菌(如粪杆菌)在盲肠中逐渐被 E. maxima 抑制。另一方面,在急性感染期间,回肠中的机会致病菌(如埃希氏菌、肠球菌和葡萄球菌)明显增多:重要意义:我们首次观察到肠道微生物群对大肠埃默氏菌感染的动态反应,并与其生命周期同步。在早期感染期间,回肠和盲肠微生物群发生的变化极小,而在急性感染和肠粘膜破坏时,回肠和盲肠微生物群会发生显著变化。当动物从球虫病中恢复过来时,肠道微生物群基本恢复正常。大肠埃希氏菌诱发的肠道炎症很可能创造了一个有利于耐气厌氧菌(如乳酸杆菌)以及兼性厌氧菌(如埃希氏菌、肠球菌和葡萄球菌)生长的环境,同时抑制了强制性厌氧菌(如产短链脂肪酸的细菌)的生长。这些发现拓展了我们对艾美耳菌感染期间微生物群结构的时间动态的了解,并提供了对球虫病发病机理的见解,支持了在控制和预防这种疾病时采用基于微生物组的策略的合理性。
Dynamic response of the intestinal microbiome to Eimeria maxima-induced coccidiosis in chickens.
Eimeria maxima is a major cause of coccidiosis in chickens and a key predisposing factor for other economically significant diseases such as necrotic enteritis. However, a detailed understanding of the intestinal microbiome response to E. maxima infection is still lacking. This study aimed to comprehensively investigate the dynamic changes of the intestinal microbiome for 14 days post-infection (dpi) with E. maxima. Bacterial 16S rRNA gene sequencing was performed with the ileal and cecal digesta collected from mock and E. maxima-infected chickens at the prepatent (3 dpi), acute (5 and 7 dpi), and recovery phases (10 and 14 dpi) of infection. Although no notable changes were observed at 3 dpi, significant alterations of the microbiota occurred in both the ileum and cecum at 5 and 7 dpi. By 14 dpi, the intestinal microbiota tended to return to a healthy state. Notably, Lactobacillus was enriched in response to E. maxima infection in both the ileum and cecum, although individual Lactobacillus, Ligilactobacillus, and Limosilactobacillus species varied in the temporal pattern of response. Concurrently, major short-chain fatty acid-producing bacteria, such as Faecalibacterium, were progressively suppressed by E. maxima in the cecum. On the other hand, opportunistic pathogens such as Escherichia, Enterococcus, and Staphylococcus were significantly enriched in the ileum during acute infection.
Importance: We have observed for the first time the dynamic response of the intestinal microbiota to Eimeria maxima infection, synchronized with its life cycle. Minimal changes occur in both the ileal and cecal microbiota during early infection, while significant alterations coincide with acute infection and disruption of the intestinal mucosal lining. As animals recover from coccidiosis, the intestinal microbiota largely returns to normal. E. maxima-induced intestinal inflammation likely creates an environment conducive to the growth of aerotolerant anaerobes such as Lactobacillus, as well as facultative anaerobes such as Escherichia, Enterococcus, and Staphylococcus, while suppressing the growth of obligate anaerobes such as short-chain fatty acid-producing bacteria. These findings expand our understanding of the temporal dynamics of the microbiota structure during Eimeria infection and offer insights into the pathogenesis of coccidiosis, supporting the rationale for microbiome-based strategies in the control and prevention of this condition.
期刊介绍:
Microbiology Spectrum publishes commissioned review articles on topics in microbiology representing ten content areas: Archaea; Food Microbiology; Bacterial Genetics, Cell Biology, and Physiology; Clinical Microbiology; Environmental Microbiology and Ecology; Eukaryotic Microbes; Genomics, Computational, and Synthetic Microbiology; Immunology; Pathogenesis; and Virology. Reviews are interrelated, with each review linking to other related content. A large board of Microbiology Spectrum editors aids in the development of topics for potential reviews and in the identification of an editor, or editors, who shepherd each collection.