Tight Regulation of Extracellular Superoxide Points to Its Vital Role in the Physiology of the Globally Relevant Roseobacter Clade
Tight Regulation of Extracellular Superoxide Points to Its Vital Role in the Physiology of the Globally Relevant Roseobacter Clade
复制标题
DOI：
10.1128/mbio.02668-18
复制
发表时间：
2019-03-01
期刊：
影响因子：
6.4
通讯作者：
Plummer, Sydney
中科院分区：
文献类型：
--
作者：
Hansel, Colleen M.;Diaz, Julia M.;Plummer, Sydney
在动物和植物生理学中，越来越多的人认识到活性氧（ROS）过氧化物不仅有害，而且对生命至关重要。然而，尽管健康的细菌和浮游植物广泛产生胞外超氧化物，这种分子仍然与压力和死亡有关。在这里，我们量化细胞外超氧化物的生产由七个生态不同的细菌内的Roseelae分支，并专门针对两个物种的细胞外超氧化物和生理之间的联系。我们揭示了所有物种的细胞归一化超氧化物的产生速率和细胞数量之间的强烈的反比关系。对于指数增长的细胞Ruegeria pomeroyi DSS-3和Roseopathy sp.菌株AzwK-3b，我们表明，超氧化物水平的调节响应于细胞密度通过快速调制的总产量，而不是衰减。在分批培养的生命周期中，细胞外超氧化物水平通过生产和衰变过程的平衡进行严格调节，允许在活跃生长期间接近恒定的超氧化物水平和进入稳定期后的最低水平。此外，通过在生长期间添加外源性超氧化物歧化酶来去除超氧化物导致显著的生长抑制。总的来说，这些结果表明，严格的监管胞外超氧化物的代表性成员的Roseoprotein进化枝，与超氧化物在生长调节中的作用一致，广泛承认在真菌，动物和植物physiology.IMPORTANCE形成的活性氧（ROS）通过部分减少分子氧广泛与微生物和海洋系统内的压力。然而，对健康和活跃生长的海洋细菌和浮游植物产生ROS超氧化物的广泛观察使人们对超氧化物在海洋微生物的健康和生理学中的作用提出了质疑。在这里，我们表明，超氧化物是由几个海洋细菌内广泛和丰富的Rosebellum分支。细胞外的超氧化物水平通过响应于分批培养中的细胞密度和生命阶段的生产和衰变过程的严格调节平衡来控制。细胞外超氧化物的去除导致实质性的生长抑制。这些发现指出了超氧化物在这个无处不在的微生物群体的健康和生长中的重要作用，并且可能超越。
There is a growing appreciation within animal and plant physiology that the reactive oxygen species (ROS) superoxide is not only detrimental but also essential for life. Yet, despite widespread production of extracellular superoxide by healthy bacteria and phytoplankton, this molecule remains associated with stress and death. Here, we quantify extracellular superoxide production by seven ecologically diverse bacteria within the Roseobacter clade and specifically target the link between extracellular superoxide and physiology for two species. We reveal for all species a strong inverse relationship between cell-normalized superoxide production rates and cell number. For exponentially growing cells of Ruegeria pomeroyi DSS-3 and Roseobacter sp. strain AzwK-3b, we show that superoxide levels are regulated in response to cell density through rapid modulation of gross production and not decay. Over a life cycle of batch cultures, extracellular superoxide levels are tightly regulated through a balance of both production and decay processes allowing for nearly constant levels of superoxide during active growth and minimal levels upon entering stationary phase. Further, removal of superoxide through the addition of exogenous superoxide dismutase during growth leads to significant growth inhibition. Overall, these results point to tight regulation of extracellular superoxide in representative members of the Roseobacter clade, consistent with a role for superoxide in growth regulation as widely acknowledged in fungal, animal, and plant physiology.IMPORTANCE Formation of reactive oxygen species (ROS) through partial reduction of molecular oxygen is widely associated with stress within microbial and marine systems. Nevertheless, widespread observations of the production of the ROS superoxide by healthy and actively growing marine bacteria and phytoplankton call into question the role of superoxide in the health and physiology of marine microbes. Here, we show that superoxide is produced by several marine bacteria within the widespread and abundant Roseobacter clade. Superoxide levels outside the cell are controlled via a tightly regulated balance of production and decay processes in response to cell density and life stage in batch culture. Removal of extracellular superoxide leads to substantial growth inhibition. These findings point to an essential role for superoxide in the health and growth of this ubiquitous group of microbes, and likely beyond.