Department of Biology, Indiana University, Bloomington, Indiana, USA
Department of Biology, Indiana University, Bloomington, Indiana, USA.
mBio. 2018 Jul 3;9(4):e00780-18. doi: 10.1128/mBio.00780-18.
In bacteria and eukaryotes alike, proper cellular physiology relies on robust subcellular organization. For the phototrophic purple nonsulfur bacteria (PNSB), this organization entails the use of a light-harvesting, membrane-bound compartment known as the intracytoplasmic membrane (ICM). Here we show that ICMs are spatially and temporally localized in diverse patterns among PNSB. We visualized ICMs in live cells of 14 PNSB species across nine genera by exploiting the natural autofluorescence of the photosynthetic pigment bacteriochlorophyll (BChl). We then quantitatively characterized ICM localization using automated computational analysis of BChl fluorescence patterns within single cells across the population. We revealed that while many PNSB elaborate ICMs along the entirety of the cell, species across as least two genera restrict ICMs to discrete, nonrandom sites near cell poles in a manner coordinated with cell growth and division. Phylogenetic and phenotypic comparisons established that ICM localization and ICM architecture are not strictly interdependent and that neither trait fully correlates with the evolutionary relatedness of the species. The natural diversity of ICM localization revealed herein has implications for both the evolution of phototrophic organisms and their light-harvesting compartments and the mechanisms underpinning spatial organization of bacterial compartments. Many bacteria organize their cellular space by constructing subcellular compartments that are arranged in specific, physiologically relevant patterns. The purple nonsulfur bacteria (PNSB) utilize a membrane-bound compartment known as the intracytoplasmic membrane (ICM) to harvest light for photosynthesis. It was previously unknown whether ICM localization within cells is systematic or irregular and if ICM localization is conserved among PNSB. Here we surveyed ICM localization in diverse PNSB and show that ICMs are spatially organized in species-specific patterns. Most strikingly, several PNSB resolutely restrict ICMs to regions near the cell poles, leaving much of the cell devoid of light-harvesting machinery. Our results demonstrate that bacteria of a common lifestyle utilize unequal portions of their intracellular space to harvest light, despite light harvesting being a process that is intuitively influenced by surface area. Our findings therefore raise fundamental questions about ICM biology and evolution.
在细菌和真核生物中，细胞的正常生理功能依赖于强大的亚细胞组织。对于光养型紫色非硫细菌（PNSB）来说，这种组织需要使用一个称为细胞内膜（ICM）的光捕获、膜结合隔室。在这里，我们展示了 ICM 在不同的 PNSB 物种中以不同的空间和时间模式定位。我们通过利用光合色素细菌叶绿素（BChl）的天然自发荧光，在 14 种 PNSB 属的 9 个属的 14 个 PNSB 种的活细胞中观察 ICM。然后，我们使用单细胞内 BChl 荧光模式的自动计算分析，对 ICM 定位进行了定量描述。我们发现，虽然许多 PNSB 沿着细胞的整个长度详细阐述了 ICM，但至少有两个属的物种将 ICM 限制在靠近细胞极的离散、非随机位置，这种方式与细胞生长和分裂协调一致。系统发育和表型比较表明，ICM 定位和 ICM 结构并非严格相互依赖，并且这两个特征都不完全与物种的进化关系相关。本文揭示的 ICM 定位的自然多样性对光养生物及其光捕获隔室的进化以及细菌隔室空间组织的机制都有影响。许多细菌通过构建按特定、生理相关模式排列的亚细胞隔室来组织其细胞空间。紫色非硫细菌（PNSB）利用一种称为细胞内膜（ICM）的膜结合隔室来收集光合作用的光。以前人们不知道细胞内的 ICM 定位是系统的还是不规则的，以及 ICM 定位是否在 PNSB 中保守。在这里，我们调查了不同 PNSB 中的 ICM 定位，并显示 ICM 以特定物种特有的模式进行空间组织。最引人注目的是，一些 PNSB 坚决将 ICM 限制在靠近细胞极的区域，使细胞的大部分区域没有光捕获装置。我们的结果表明，尽管光捕获是一个直观上受表面积影响的过程，但具有共同生活方式的细菌仍会利用其细胞内空间的不同部分来收集光。因此，我们的研究结果提出了关于 ICM 生物学和进化的基本问题。
