Origin and Evolution of Carboxysome Positioning Systems in Cyanobacteria

Origin and Evolution of Carboxysome Positioning Systems in Cyanobacteria
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DOI:
10.1093/molbev/msz308
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发表时间:
2020-05-01
影响因子:
10.7
通讯作者:
Vecchiarelli, Anthony G.
Vecchiarelli, Anthony G.
中科院分区:
生物学1区
文献类型:
--
作者:
MacCready, Joshua S.;Basalla, Joseph L.;Vecchiarelli, Anthony G.

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羧基体是一种蛋白质细胞器,是蓝藻固定二氧化碳所必需的。先前,我们鉴定了一种双组分系统McdAB,其负责在模型蓝细菌细长聚球藻PCC 7942中等距定位羧基体(MacCready JS,Hakim P,Young EJ,Hu L,Liu J,Osteryoung KW,Vecchiarelli AG,Ducat DC. 2018.蛋白质梯度在类核上定位蓝藻的碳固定细胞器。eLife 7:pii:e39723)。McdA是一种ParA型ATP酶,在ATP存在下非特异性结合类核。McdB是一种直接结合羧基体的新型因子,它取代了类核中的McdA。去除McdA从类核在附近的carboxysomes由McdB导致的全球性中断McdA的对称性,和carboxysomes运动发生通过布朗棘轮为基础的机制向最高浓度的McdA。尽管蓝藻的重要性,正确定位其carboxysomes,是否McdAB系统是广泛的蓝藻仍然是一个悬而未决的问题。在这里,我们表明McdAB系统在β-蓝细菌中广泛存在,通常与碳氧体相关成分聚集在一起,而在α-蓝细菌中不存在。此外,我们表明,两个不同的McdAB系统存在于β-蓝藻,2型系统是最古老和丰富的,和1型系统,如S。细长型可能是最近才获得的最后,所有McdB蛋白质都具有能够进行液-液相分离的蛋白质的序列特征。事实上,我们发现两种McdB类型的代表在体外进行液-液相分离,这是ParA型ATP酶伴侣蛋白表现出这种行为的第一个例子。我们的研究结果有更广泛的意义,了解羧基体进化,生物发生,稳态,定位在蓝藻。
Carboxysomes are protein-based organelles that are essential for allowing cyanobacteria to fix CO2. Previously, we identified a two-component system, McdAB, responsible for equidistantly positioning carboxysomes in the model cyanobacterium Synechococcus elongatus PCC 7942 (MacCready JS, Hakim P, Young EJ, Hu L, Liu J, Osteryoung KW, Vecchiarelli AG, Ducat DC. 2018. Protein gradients on the nucleoid position the carbon-fixing organelles of cyanobacteria. eLife 7:pii:e39723). McdA, a ParA-type ATPase, nonspecifically binds the nucleoid in the presence of ATP. McdB, a novel factor that directly binds carboxysomes, displaces McdA from the nucleoid. Removal of McdA from the nucleoid in the vicinity of carboxysomes by McdB causes a global break in McdA symmetry, and carboxysome motion occurs via a Brownian-ratchet-based mechanism toward the highest concentration of McdA. Despite the importance for cyanobacteria to properly position their carboxysomes, whether the McdAB system is widespread among cyanobacteria remains an open question. Here, we show that the McdAB system is widespread among beta-cyanobacteria, often clustering with carboxysome-related components, and is absent in alpha-cyanobacteria. Moreover, we show that two distinct McdAB systems exist in beta-cyanobacteria, with Type 2 systems being the most ancestral and abundant, and Type 1 systems, like that of S. elongatus, possibly being acquired more recently. Lastly, all McdB proteins share the sequence signatures of a protein capable of undergoing liquid-liquid phase separation. Indeed, we find that representatives of both McdB types undergo liquid-liquid phase separation in vitro, the first example of a ParA-type ATPase partner protein to exhibit this behavior. Our results have broader implications for understanding carboxysome evolution, biogenesis, homeostasis, and positioning in cyanobacteria.