Zhang Zhihong, Wang Kaiming, Oh Jee-Hwan, Zhang Shenwei, van Pijkeren Jan-Peter, Cheng Christopher C, Ren Dayong, Wei Hua, Gänzle Michael G, Walter Jens
State Key Laboratory of Food Science and Technology, Nanchang University, Nanchang, China.
Agricultural, Food and Nutritional Science, University of Alberta, Edmonton, AB, Canada.
Front Microbiol. 2020 Dec 21;11:601422. doi: 10.3389/fmicb.2020.601422. eCollection 2020.
Lineages within the species have specialized to various hosts and their genomes reflect these adaptations. The gene cluster is conserved in most human and poultry isolates but is infrequent in rodent and porcine isolates. This gene cluster confers the transformation of glycerol into 3-hydroxy-propionaldehyde (reuterin), which can either be secreted and function as precursor of the antimicrobial compound acrolein or serve as an electron acceptor that enhances the organisms' growth rate. However, it remains unclear which of these two functions is more relevant for evolution and ecology. Here we characterized the effect of glycerol on growth rate and reuterin formation in strains across different phylogenetic lineages during growth on ecologically relevant carbohydrates. We further evaluated the innate reuterin resistance among these strains to infer a possible role of reuterin in the evolution of strains. Results revealed that the poultry/human lineage VI strain, DSM 17938 shows more growth enhancement through glycerol and greater capacity for reuterin production on glucose and maltose as compared to human lineage II strains. Interestingly, reuterin production in lineage II strains was significantly elevated on raffinose and lactose, reaching levels similar to DSM 17938. On all carbohydrates tested, reuterin production occurred during the exponential growth phase and became undetectable during the stationary growth phase. The amount of reuterin produced was sufficient to inhibit , suggesting that it could be ecologically relevant, but the resistance towards reuterin among strains was highly variable and, for the most part, unrelated to the strain's capacity for reuterin production. Overall, the findings suggest differences in the substrate-specific regulation of the cluster in lineages that might be reflective of their ecological niches, e.g., chicken foregut versus human infant and adult large intestine. Such information can inform future studies on the ecology of and guide the development of synbiotic applications to improve the therapeutic use of this species.
该物种内的谱系已专门适应各种宿主,其基因组反映了这些适应性变化。该基因簇在大多数人类和家禽分离株中是保守的,但在啮齿动物和猪的分离株中很少见。这个基因簇能将甘油转化为3-羟基丙醛(罗伊氏菌素),它既可以分泌出来,作为抗菌化合物丙烯醛的前体发挥作用,也可以作为电子受体,提高生物体的生长速率。然而,目前尚不清楚这两种功能中哪一种对进化和生态更为重要。在这里,我们描述了甘油对不同系统发育谱系的菌株在与生态相关的碳水化合物上生长时的生长速率和罗伊氏菌素形成的影响。我们进一步评估了这些菌株对罗伊氏菌素的天然抗性,以推断罗伊氏菌素在菌株进化中的可能作用。结果显示,与人类谱系II菌株相比,家禽/人类谱系VI菌株DSM 17938在葡萄糖和麦芽糖上通过甘油表现出更多的生长促进作用以及更大的罗伊氏菌素产生能力。有趣的是,谱系II菌株在棉子糖和乳糖上的罗伊氏菌素产量显著提高,达到了与DSM 17938相似的水平。在所有测试的碳水化合物上,罗伊氏菌素的产生都发生在指数生长期,在稳定生长期则检测不到。产生的罗伊氏菌素量足以产生抑制作用,这表明它可能具有生态相关性,但菌株对罗伊氏菌素的抗性高度可变,并且在很大程度上与菌株产生罗伊氏菌素的能力无关。总体而言,这些发现表明该基因簇在不同谱系中的底物特异性调控存在差异,这可能反映了它们的生态位,例如鸡前肠与人类婴儿和成人的大肠。这些信息可以为未来关于该物种生态学的研究提供参考,并指导合生元应用的开发,以改善该物种的治疗用途。