Nugraha Dendi Krisna, Nishida Takashi, Tamaki Yuki, Hiramatsu Yukihiro, Yamaguchi Hiroyuki, Horiguchi Yasuhiko
Department of Molecular Bacteriology, Research Institute for Microbial Diseases, Osaka University, Suita, Osaka, Japan.
Department of Medical Laboratory Science, Faculty of Health Sciences, Hokkaido University, Sapporo, Hokkaido, Japan.
Microbiol Spectr. 2023 Mar 27;11(2):e0048723. doi: 10.1128/spectrum.00487-23.
The respiratory pathogenic bacterium Bordetella bronchiseptica can persistently survive in terrestrial and aquatic environments, providing a source of infection. However, the environmental lifestyle of the bacterium is poorly understood. In this study, expecting repeated encounters of the bacteria with environmental protists, we explored the interaction between B. bronchiseptica and a representative environmental amoeba, Acanthamoeba castellanii, and found that the bacteria resisted amoeba digestion and entered contractile vacuoles (CVs), which are intracellular compartments involved in osmoregulation, to escape amoeba cells. In prolonged coculture, A. castellanii supported the proliferation of B. bronchiseptica. The avirulent Bvg phase, but not the virulent Bvg phase, of the bacteria was advantageous for survival in the amoebae. We further demonstrate that two Bvg phase-specific virulence factors, filamentous hemagglutinin and fimbriae, were targeted for predation by A. castellanii. These results are evidence that the BvgAS two-component system, the master regulator for Bvg phase conversion, plays an indispensable role in the survival of B. bronchiseptica in amoebae. The pathogenic bacterium Bordetella bronchiseptica, which causes respiratory diseases in various mammals, exhibits distinct Bvg and Bvg phenotypes. The former represents the virulent phase, in which the bacteria express a set of virulence factors, while the role of the latter in the bacterial life cycle remains to be understood. In this study, we demonstrate that B. bronchiseptica in the Bvg phase, but not the Bvg phase, survives and proliferates in coculture with Acanthamoeba castellanii, an environmental amoeba. Two Bvg phase-specific virulence factors, filamentous hemagglutinin and fimbriae, were targeted by A. castellanii predation. B. bronchiseptica turns into the Bvg phase at temperatures in which the bacteria normally encounter these amoebae. These findings demonstrate that the Bvg phase of B. bronchiseptica is advantageous for survival outside mammalian hosts and that the bacteria can utilize protists as transient hosts in natural environments.
呼吸道病原菌支气管败血波氏杆菌可在陆地和水生环境中持续存活，成为感染源。然而，人们对该细菌的环境生存方式了解甚少。在本研究中，鉴于预计细菌会反复与环境中的原生生物相遇，我们探究了支气管败血波氏杆菌与一种典型的环境变形虫——卡氏棘阿米巴之间的相互作用，发现该细菌能够抵抗变形虫的消化，并进入参与渗透调节的细胞内区室收缩泡，从而逃离变形虫细胞。在长时间共培养中，卡氏棘阿米巴支持支气管败血波氏杆菌的增殖。该细菌的无毒Bvg相而非有毒Bvg相有利于在变形虫中存活。我们进一步证明，两种Bvg相特异性毒力因子，即丝状血凝素和菌毛，成为卡氏棘阿米巴捕食的目标。这些结果证明，BvgAS双组分系统作为Bvg相转换的主要调节因子，在支气管败血波氏杆菌在变形虫中的存活中起着不可或缺的作用。致病性细菌支气管败血波氏杆菌可在多种哺乳动物中引发呼吸道疾病，表现出不同的Bvg +和Bvg -表型。前者代表有毒阶段，在此阶段细菌表达一组毒力因子，而后者在细菌生命周期中的作用仍有待了解。在本研究中，我们证明处于Bvg -相而非Bvg +相的支气管败血波氏杆菌在与环境变形虫卡氏棘阿米巴共培养时能够存活并增殖。两种Bvg相特异性毒力因子，丝状血凝素和菌毛，成为卡氏棘阿米巴捕食的目标。支气管败血波氏杆菌在通常会遇到这些变形虫的温度下转变为Bvg -相。这些发现表明，支气管败血波氏杆菌的Bvg -相对在哺乳动物宿主外的存活有利，并且该细菌可以利用原生生物作为自然环境中的临时宿主。
