Virulence as a Side Effect of Interspecies Interaction in Vibrio Coral Pathogens

Virulence as a Side Effect of Interspecies Interaction in Vibrio Coral Pathogens
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DOI:
10.1128/mbio.00201-20
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发表时间:
2020-07
期刊:
影响因子:
6.4
通讯作者:
Esther Rubio-Portillo;Ana-Belén Martín-Cuadrado;A. Caraballo-Rodríguez;F. Rohwer;P. Dorrestein;J. Antón
Esther Rubio-Portillo;Ana-Belén Martín-Cuadrado;A. Caraballo-Rodríguez;F. Rohwer;P. Dorrestein;J. Antón
中科院分区:
生物学1区
文献类型:
--
作者:
Esther Rubio-Portillo;Ana-Belén Martín-Cuadrado;A. Caraballo-Rodríguez;F. Rohwer;P. Dorrestein;J. Antón

文献摘要

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溶珊瑚弧菌(Vibrio coralliilyticus)和地中海弧菌(Vibrio medicinei)是重要的珊瑚病原菌,它们同时感染宿主时,珊瑚的危害会加重。这造成的后果是,这些病原体散布在不同的地方,可能加剧对珊瑚礁的有害影响。然而,这种协同作用的机制是未知的。这里描述的工作提供了一个新的视角,这两个弧菌珊瑚病原体之间的复杂的相互作用,这表明珊瑚感染可能是种间竞争的附带影响。这项工作的主要影响是:(i)弧菌毒力机制在没有宿主的情况下被激活,作为对种间竞争的响应;(ii)弧菌珊瑚病原体释放分子,导致珊瑚微生物组发生变化,有利于整个弧菌群落的致病潜力。因此,我们的研究结果强调,社会线索和竞争感是珊瑚疾病发展的关键决定因素。由弧菌病原体引起的珊瑚疾病爆发的流行率和严重性的增加,以及与全球变暖有关的珊瑚疾病爆发,严重影响了整个海洋的造礁珊瑚。珊瑚Oculina patagonica已被用作一个模型系统,研究珊瑚漂白弧菌感染。以往的资料表明,当两种珊瑚病原菌(溶珊瑚弧菌和地中海弧菌)同时感染O。patagonica,它们的致病性大于当每种细菌单独感染时。在这里,为了理解这种协同效应的机制,进行了单培养和共培养的转录组学分析以及实验感染实验。我们的结果显示,在培养条件下两种弧菌之间的相互作用过表达毒力因子基因(例如,编码铁载体、VI型分泌系统和毒素等的那些)。此外,在这些条件下,弧菌也更容易形成生物膜或通过诱导侧鞭毛变得能动。所有这些变化都是对竞争物种存在的生理反应,当它们存在于混合种群中时,可能有利于宿主的定殖。此外,在珊瑚实验感染过程中,我们发现珊瑚暴露于溶珊瑚弧菌和地中海弧菌共培养过程中释放的分子会引起珊瑚微生物组的变化,有利于珊瑚组织的损伤,并增加溶血血小板活化因子的产生。因此,我们建议,竞争传感,定义为检测伤害或竞争弧菌物种的存在的生理反应,增强了珊瑚弧菌病原体入侵宿主并导致组织坏死的能力。重要性溶珊瑚弧菌和地中海弧菌是重要的珊瑚病原体,能够引起严重的珊瑚损害,当它们同时感染宿主时,损害会严重增加。这造成的后果是,这些病原体散布在不同的地方,可能加剧对珊瑚礁的有害影响。然而,这种协同作用的机制是未知的。这里描述的工作提供了一个新的视角,这两个弧菌珊瑚病原体之间的复杂的相互作用,这表明珊瑚感染可能是种间竞争的附带影响。这项工作的主要影响是:(i)弧菌毒力机制在没有宿主的情况下被激活,作为对种间竞争的响应;(ii)弧菌珊瑚病原体释放分子,导致珊瑚微生物组发生变化,有利于整个弧菌群落的致病潜力。因此,我们的研究结果强调,社会线索和竞争感是珊瑚疾病发展的关键决定因素。
Vibrio coralliilyticus and Vibrio mediterranei are important coral pathogens capable of inducing serious coral damage, which increases severely when they infect the host simultaneously. This has consequences related to the dispersion of these pathogens among different locations that could enhance deleterious effects on coral reefs. However, the mechanisms underlying this synergistic interaction are unknown. The work described here provides a new perspective on the complex interactions among these two Vibrio coral pathogens, suggesting that coral infection could be a collateral effect of interspecific competition. Major implications of this work are that (i) Vibrio virulence mechanisms are activated in the absence of the host as a response to interspecific competition and (ii) release of molecules by Vibrio coral pathogens produces changes in the coral microbiome that favor the pathogenic potential of the entire Vibrio community. Thus, our results highlight that social cues and competition sensing are crucial determinants of development of coral diseases. ABSTRACT The increase in prevalence and severity of coral disease outbreaks produced by Vibrio pathogens, and related to global warming, has seriously impacted reef-building corals throughout the oceans. The coral Oculina patagonica has been used as a model system to study coral bleaching produced by Vibrio infection. Previous data demonstrated that when two coral pathogens (Vibrio coralliilyticus and Vibrio mediterranei) simultaneously infected the coral O. patagonica, their pathogenicity was greater than when each bacterium was infected separately. Here, to understand the mechanisms underlying this synergistic effect, transcriptomic analyses of monocultures and cocultures as well as experimental infection experiments were performed. Our results revealed that the interaction between the two vibrios under culture conditions overexpressed virulence factor genes (e.g., those encoding siderophores, the type VI secretion system, and toxins, among others). Moreover, under these conditions, vibrios were also more likely to form biofilms or become motile through induction of lateral flagella. All these changes that occur as a physiological response to the presence of a competing species could favor the colonization of the host when they are present in a mixed population. Additionally, during coral experimental infections, we showed that exposure of corals to molecules released during V. coralliilyticus and V. mediterranei coculture induced changes in the coral microbiome that favored damage to coral tissue and increased the production of lyso-platelet activating factor. Therefore, we propose that competition sensing, defined as the physiological response to detection of harm or to the presence of a competing Vibrio species, enhances the ability of Vibrio coral pathogens to invade their host and cause tissue necrosis. IMPORTANCE Vibrio coralliilyticus and Vibrio mediterranei are important coral pathogens capable of inducing serious coral damage, which increases severely when they infect the host simultaneously. This has consequences related to the dispersion of these pathogens among different locations that could enhance deleterious effects on coral reefs. However, the mechanisms underlying this synergistic interaction are unknown. The work described here provides a new perspective on the complex interactions among these two Vibrio coral pathogens, suggesting that coral infection could be a collateral effect of interspecific competition. Major implications of this work are that (i) Vibrio virulence mechanisms are activated in the absence of the host as a response to interspecific competition and (ii) release of molecules by Vibrio coral pathogens produces changes in the coral microbiome that favor the pathogenic potential of the entire Vibrio community. Thus, our results highlight that social cues and competition sensing are crucial determinants of development of coral diseases.