School of Life Sciences, Tokyo University of Pharmacy and Life Sciences, Hachioji, Tokyo, Japan.
Appl Environ Microbiol. 2023 Jul 26;89(7):e0086823. doi: 10.1128/aem.00868-23. Epub 2023 Jun 27.
Shewanella oneidensis MR-1 is a facultative anaerobe that grows by respiration using a variety of electron acceptors. This organism serves as a model to study how bacteria thrive in redox-stratified environments. A glucose-utilizing engineered derivative of MR-1 has been reported to be unable to grow in glucose minimal medium (GMM) in the absence of electron acceptors, despite this strain having a complete set of genes for reconstructing glucose to lactate fermentative pathways. To gain insights into why MR-1 is incapable of fermentative growth, this study examined a hypothesis that this strain is programmed to repress the expression of some carbon metabolic genes in the absence of electron acceptors. Comparative transcriptomic analyses of the MR-1 derivative were conducted in the presence and absence of fumarate as an electron acceptor, and these found that the expression of many genes involved in carbon metabolism required for cell growth, including several tricarboxylic acid (TCA) cycle genes, was significantly downregulated in the absence of fumarate. This finding suggests a possibility that MR-1 is unable to grow fermentatively on glucose in minimal media owing to the shortage of nutrients essential for cell growth, such as amino acids. This idea was demonstrated in subsequent experiments that showed that the MR-1 derivative fermentatively grows in GMM containing tryptone or a defined mixture of amino acids. We suggest that gene regulatory circuits in MR-1 are tuned to minimize energy consumption under electron acceptor-depleted conditions, and that this results in defective fermentative growth in minimal media. It is an enigma why S. oneidensis MR-1 is incapable of fermentative growth despite having complete sets of genes for reconstructing fermentative pathways. Understanding the molecular mechanisms behind this defect will facilitate the development of novel fermentation technologies for the production of value-added chemicals from biomass feedstocks, such as electro-fermentation. The information provided in this study will also improve our understanding of the ecological strategies of bacteria living in redox-stratified environments.
希瓦氏菌属（Shewanella oneidensis）MR-1 是一种兼性厌氧菌，它可以通过利用各种电子受体进行呼吸来生长。该生物体是研究细菌如何在氧化还原分层环境中茁壮成长的模型。据报道，一种利用葡萄糖的工程衍生菌尽管具有完整的基因来重建葡萄糖到乳酸发酵途径，但在没有电子受体的情况下，无法在葡萄糖最小培养基 (GMM) 中生长。为了深入了解为什么 MR-1 不能进行发酵生长，本研究检验了一个假设，即该菌株在没有电子受体的情况下被编程抑制某些碳代谢基因的表达。在存在和不存在富马酸盐作为电子受体的情况下，对 MR-1 衍生菌进行了比较转录组分析，结果发现，许多与细胞生长所需的碳代谢有关的基因的表达，包括几个三羧酸 (TCA) 循环基因，在没有富马酸盐的情况下显著下调。这一发现表明，MR-1 可能由于细胞生长所必需的营养物质（如氨基酸）短缺，无法在最小培养基中利用葡萄糖进行发酵生长。随后的实验证明了这一想法，即 MR-1 衍生菌可以在含有胰蛋白胨或氨基酸定义混合物的 GMM 中进行发酵生长。我们认为，MR-1 中的基因调控电路被调谐为在电子受体耗尽的条件下最小化能量消耗，这导致了在最小培养基中发酵生长缺陷。令人困惑的是，尽管 S. oneidensis MR-1 具有完整的基因来重建发酵途径，但它却无法进行发酵生长。了解这种缺陷背后的分子机制将有助于开发新型发酵技术，从生物质原料（如电发酵）生产有价值的化学品。本研究提供的信息还将提高我们对生活在氧化还原分层环境中的细菌的生态策略的理解。
