A Tripartite, Hierarchical Sigma Factor Cascade Promotes Hormogonium Development in the Filamentous Cyanobacterium Nostoc punctiforme
A Tripartite, Hierarchical Sigma Factor Cascade Promotes Hormogonium Development in the Filamentous Cyanobacterium Nostoc punctiforme
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DOI：
10.1128/msphere.00231-19
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发表时间：
2019-05-01
期刊：
影响因子：
4.8
通讯作者：
Risser, Douglas D.
中科院分区：
文献类型：
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作者：
Gonzalez, Alfonso;Riley, Kelsey W.;Risser, Douglas D.
蓝细菌是能够进行光合作用的原核生物，通常也能固氮。因此，它们对全球初级生产和氮循环做出了重大贡献。此外，分类学第IV和V小节中的多细胞丝状蓝藻在发育上是复杂的，表现出一系列分化的细胞类型和丝状体，包括能动的藻殖体，使它们成为研究发育的有价值的模式生物。为了研究西格玛因子在控制藻殖体发育的基因调控网络（GRN）中的作用，在丝状蓝藻模式点状念珠藻中进行了遗传学、免疫学和时间分辨转录组学分析的组合，该模式与其他常见的模式蓝藻不同，保留了田间分离株的发育复杂性。这些结果支持了一个模型，其中的Hormogonium GRN是由一个分层西格玛因子级联驱动的，sigi激活sigC和sigF的表达，以及相当大一部分额外的Hormogonium特异性基因，包括那些驱动细胞结构变化的基因。反过来，sigC调节较小的基因子集的几个过程，在促进还原性细胞分裂中起主导作用，也可以积极和消极地调节sigJ，以加强发展计划和协调基因表达的时间，分别。相比之下，sigF调节子非常有限。在藻殖体发育中具有特征性作用的基因中，只有pilA显示出严格的sigF依赖性。对于sigl依赖性基因，还鉴定了推定的共有启动子，其主要由高度保守的延伸的-10区域组成，在此称为J-Box，其广泛分布于蓝细菌谱系的不同成员中。并且它们的代谢能力加上它们易于遗传操作使它们成为用于诸如生物材料和生物肥料生产的有吸引力的平台。实现这些目标可能需要对这些生物的GRN进行详细的了解和精确的重新布线。丝状蓝藻复杂的表型可塑性也使它们成为原核发育的有价值的模型。然而，目前的研究受到限制，主要集中在少数模式菌株，未能反映外地同行的表型，可能限制生物技术的进步和更全面的了解发育的复杂性。在这里，使用念珠藻punctiforme，一个模型丝状蓝藻，保留野生菌株的发展范围，我们定义了以前未知的明确的作用，为三个西格玛因素在藻殖体的发展。这些发现大大推进了我们对蓝藻发育和基因调控的理解，并可用于未来的应用。
Cyanobacteria are prokaryotes capable of oxygenic photosynthesis, and frequently, nitrogen fixation as well. As a result, they contribute substantially to global primary production and nitrogen cycles. Furthermore, the multicellular filamentous cyanobacteria in taxonomic subsections IV and V are developmentally complex, exhibiting an array of differentiated cell types and filaments, including motile hormogonia, making them valuable model organisms for studying development. To investigate the role of sigma factors in the gene regulatory network (GRN) controlling hormogonium development, a combination of genetic, immunological, and time-resolved transcriptomic analyses were conducted in the model filamentous cyanobacterium Nostoc punctiforme, which, unlike other common model cyanobacteria, retains the developmental complexity of field isolates. The results support a model where the hormogonium GRN is driven by a hierarchal sigma factor cascade, with sigi activating the expression of both sigC and sigF, as well as a substantial portion of additional hormogonium-specific genes, including those driving changes to cellular architecture. In turn, sigC regulates smaller subsets of genes for several processes, plays a dominant role in promoting reductive cell division, and may also both positively and negatively regulate sigJ to reinforce the developmental program and coordinate the timing of gene expression, respectively. In contrast, the sigF regulon is extremely limited. Among genes with characterized roles in hormogonium development, only pilA shows stringent sigF dependence. For sigl-dependent genes, a putative consensus promoter was also identified, consisting primarily of a highly conserved extended -10 region, here designated a J-Box, which is widely distributed among diverse members of the cyanobacterial lineage.IMPORTANCE Cyanobacteria are integral to global carbon and nitrogen cycles, and their metabolic capacity coupled with their ease of genetic manipulation make them attractive platforms for applications such as biomaterial and biofertilizer production. Achieving these goals will likely require a detailed understanding and precise rewiring of these organisms' GRNs. The complex phenotypic plasticity of filamentous cyanobacteria has also made them valuable models of prokaryotic development. However, current research has been limited by focusing primarily on a handful of model strains which fail to reflect the phenotypes of field counterparts, potentially limiting biotechnological advances and a more comprehensive understanding of developmental complexity. Here, using Nostoc punctiforme, a model filamentous cyanobacterium that retains the developmental range of wild isolates, we define previously unknown definitive roles for a trio of sigma factors during hormogonium development. These findings substantially advance our understanding of cyanobacterial development and gene regulation and could be leveraged for future applications.