Dupont Charly A, Bourigault Yvann, Osmond Théo, Nier Maëva, Barbey Corinne, Latour Xavier, Konto-Ghiorghi Yoan, Verdon Julien, Merieau Annabelle
Laboratoire de Communication Bactérienne et Stratégies Anti-infectieuses (CBSA UR), Univ Rouen Normandie, Université Caen Normandie, Normandie Univ, Rouen, France.
Structure Fédérative de Recherche Normandie Végétale and Entente Franco-Québécoise NOR-SEVE, NORVEGE, Rouen, France.
Front Microbiol. 2023 Oct 16;14:1264801. doi: 10.3389/fmicb.2023.1264801. eCollection 2023.
Bacterial communication is a fundamental process used to synchronize gene expression and collective behavior among the bacterial population. The most studied bacterial communication system is quorum sensing, a cell density system, in which the concentration of inductors increases to a threshold level allowing detection by specific receptors. As a result, bacteria can change their behavior in a coordinated way. While in quorum sensing based on the synthesis of -acyl homoserine lactone molecules is well studied, volatile organic compounds, although considered to be communication signals in the rhizosphere, are understudied. The MFE01 strain has a very active type six secretion system that can kill some competitive bacteria. Furthermore, MFE01 emits numerous volatile organic compounds, including 1-undecene, which contributes to the aerial inhibition of growth. Finally, MFE01 appears to be deprived of -acyl homoserine lactone synthase. The main objective of this study was to explore the role of 1-undecene in the communication of MFE01. We constructed a mutant affected in gene encoding the enzyme responsible for 1-undecene synthesis to provide further insight into the role of 1-undecene in MFE01. First, we studied the impacts of this mutation both on volatile organic compounds emission, using headspace solid-phase microextraction combined with gas chromatography-mass spectrometry and on long-range inhibition. Then, we analyzed influence of 1-undecene on MFE01 coordinated phenotypes, including type six secretion system activity and biofilm formation. Next, to test the ability of MFE01 to synthesize -acyl homoserine lactones in our conditions, we investigated the presence of corresponding genes across the MFE01 genome and we exposed its biofilms to an acyl homoserine lactone-degrading enzyme. Finally, we examined the effects of 1-undecene emission on MFE01 biofilm maturation and aerial communication using an original experimental set-up. This study demonstrated that the Δ mutant is impaired in biofilm maturation. An exposure of the Δ mutant to the volatile compounds emitted by MFE01 during the biofilm development restored the biofilm maturation process. These findings indicate that MFE01 uses 1-undecene emission for aerial communication, reporting for the first time this volatile organic compound as bacterial intraspecific communication signal.
细菌通讯是一种基本过程，用于使细菌群体中的基因表达和集体行为同步。研究最多的细菌通讯系统是群体感应，这是一种细胞密度系统，其中诱导物的浓度增加到阈值水平，以便被特定受体检测到。结果，细菌能够以协调的方式改变其行为。虽然基于酰基高丝氨酸内酯分子合成的群体感应已得到充分研究，但挥发性有机化合物尽管被认为是根际中的通讯信号，却研究不足。MFE01菌株具有非常活跃的VI型分泌系统，能够杀死一些竞争性细菌。此外，MFE01会释放大量挥发性有机化合物，包括1-十一碳烯，这有助于对生长产生气生抑制作用。最后，MFE01似乎缺乏酰基高丝氨酸内酯合酶。本研究的主要目的是探究1-十一碳烯在MFE01通讯中的作用。我们构建了一个在编码负责1-十一碳烯合成的酶的基因中发生突变的突变体，以进一步深入了解1-十一碳烯在MFE01中的作用。首先，我们使用顶空固相微萃取结合气相色谱-质谱联用技术研究了这种突变对挥发性有机化合物排放以及长距离抑制的影响。然后，我们分析了1-十一碳烯对MFE01协调表型的影响，包括VI型分泌系统活性和生物膜形成。接下来，为了测试MFE01在我们的条件下合成酰基高丝氨酸内酯的能力，我们研究了MFE01基因组中相应基因的存在情况，并将其生物膜暴露于一种酰基高丝氨酸内酯降解酶中。最后，我们使用一种原始实验装置研究了1-十一碳烯排放对MFE01生物膜成熟和气生通讯的影响。这项研究表明，Δ突变体在生物膜成熟方面受损。在生物膜发育过程中将Δ突变体暴露于MFE01释放的挥发性化合物中可恢复生物膜成熟过程。这些发现表明，MFE01利用1-十一碳烯排放进行气生通讯，首次将这种挥发性有机化合物报道为细菌种内通讯信号。
