Department of Microbiology, University of Tennessee, Knoxville, Tennessee, USA.
PLoS One. 2011 Feb 3;6(2):e16805. doi: 10.1371/journal.pone.0016805.
The phytoplankton community in the oligotrophic open ocean is numerically dominated by the cyanobacterium Prochlorococcus, accounting for approximately half of all photosynthesis. In the illuminated euphotic zone where Prochlorococcus grows, reactive oxygen species are continuously generated via photochemical reactions with dissolved organic matter. However, Prochlorococcus genomes lack catalase and additional protective mechanisms common in other aerobes, and this genus is highly susceptible to oxidative damage from hydrogen peroxide (HOOH). In this study we showed that the extant microbial community plays a vital, previously unrecognized role in cross-protecting Prochlorococcus from oxidative damage in the surface mixed layer of the oligotrophic ocean. Microbes are the primary HOOH sink in marine systems, and in the absence of the microbial community, surface waters in the Atlantic and Pacific Ocean accumulated HOOH to concentrations that were lethal for Prochlorococcus cultures. In laboratory experiments with the marine heterotroph Alteromonas sp., serving as a proxy for the natural community of HOOH-degrading microbes, bacterial depletion of HOOH from the extracellular milieu prevented oxidative damage to the cell envelope and photosystems of co-cultured Prochlorococcus, and facilitated the growth of Prochlorococcus at ecologically-relevant cell concentrations. Curiously, the more recently evolved lineages of Prochlorococcus that exploit the surface mixed layer niche were also the most sensitive to HOOH. The genomic streamlining of these evolved lineages during adaptation to the high-light exposed upper euphotic zone thus appears to be coincident with an acquired dependency on the extant HOOH-consuming community. These results underscore the importance of (indirect) biotic interactions in establishing niche boundaries, and highlight the impacts that community-level responses to stress may have in the ecological and evolutionary outcomes for co-existing species.
贫营养开阔海域的浮游植物群落中,数量上占优势的是蓝细菌原绿球藻,其光合作用约占总量的一半。在原绿球藻生长的光照层中,活性氧会通过与溶解有机物的光化学反应不断产生。然而,原绿球藻基因组缺乏过氧化氢酶和其他好氧生物中常见的额外保护机制,因此该属极易受到过氧化氢(HOOH)的氧化损伤。在这项研究中,我们表明,现存的微生物群落对于保护贫营养开阔海域表水层中的原绿球藻免受氧化损伤起着至关重要的、以前未被认识到的作用。微生物是海洋系统中 HOOH 的主要消耗者,如果没有微生物群落,大西洋和太平洋的表层水会积累到足以杀死原绿球藻培养物的 HOOH 浓度。在以海洋异养菌交替单胞菌为代表的自然 HOOH 降解微生物群落的实验室实验中,细菌从细胞外环境中去除 HOOH,防止了共培养的原绿球藻的细胞膜和光合系统受到氧化损伤,并促进了原绿球藻在生态相关的细胞浓度下的生长。奇怪的是,最近进化的原绿球藻谱系利用表水层小生境,对 HOOH 也最为敏感。这些进化谱系在适应高光暴露上层真光层过程中的基因组简化,似乎与对现存的 HOOH 消耗微生物群落的获得性依赖同时发生。这些结果强调了(间接)生物相互作用在确定生态位边界方面的重要性,并突出了群落水平对压力的响应可能对共存物种的生态和进化结果产生的影响。