The diversification and lineage-specific expansion of nitric oxide signaling in Placozoa: insights in the evolution of gaseous transmission

The diversification and lineage-specific expansion of nitric oxide signaling in Placozoa: insights in the evolution of gaseous transmission
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DOI:
10.1038/s41598-020-69851-w
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发表时间:
2020-08-03
期刊:
影响因子:
4.6
通讯作者:
Fasshauer,Dirk
Fasshauer,Dirk
中科院分区:
综合性期刊3区
文献类型:
--
作者:
Moroz,Leonid L.;Romanova,Daria Y.;Fasshauer,Dirk

文献摘要

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一氧化氮(NO)是一种普遍存在的气体信使,但我们对它的早期演化知之甚少。在这里,我们分析了一氧化氮合酶(NOS)在四个不同种类的扁形动物的早期分支的动物谱系之一。与其他研究的无脊椎动物相比,Trichoplax和Hoilungia有三个不同的NOS基因,包括含PDZ结构域的NOS。使用超灵敏的毛细管电泳分析,我们量化了亚硝酸盐(NO氧化的产物)和l-瓜氨酸(从l-精氨酸合成NO的副产物),它们受到NOS抑制剂的影响,证实了Trichoplax中存在功能酶。使用荧光单分子原位杂交,我们发现,不同的NOS表达在不同的细胞亚群,与一个显着的分布接近的边缘区域ofTrichoplax。这些数据表明,分区释放的NO和更大的多样性的细胞类型比预期的扁形动物。NO受体机制包括典型的和新型的含有可溶性鸟苷酸环化酶的NIT结构域,作为推定的NO/亚硝酸盐/硝酸盐传感器。因此,尽管Trichoplax和Hoilungia是形态学上最简单的自由生活动物,但在Placozoa中NO-cGMP介导的信号传导的复杂性比在脊椎动物中更大。这种情况阐明了多个谱系特异性的多样化的NOS和NO/亚硝酸盐/硝酸盐传感器从后生动物的共同祖先和原核祖先的保守NOS架构的保存。
Nitric oxide (NO) is a ubiquitous gaseous messenger, but we know little about its early evolution. Here, we analyzed NO synthases (NOS) in four different species of placozoans—one of the early-branching animal lineages. In contrast to other invertebrates studied,TrichoplaxandHoilungiahave three distinct NOS genes, including PDZ domain-containing NOS. Using ultra-sensitive capillary electrophoresis assays, we quantified nitrites (products of NO oxidation) andl-citrulline (co-product of NO synthesis froml-arginine), which were affected by NOS inhibitors confirming the presence of functional enzymes inTrichoplax. Using fluorescent single-molecule in situ hybridization, we showed that distinct NOSs are expressed in different subpopulations of cells, with a noticeable distribution close to the edge regions ofTrichoplax. These data suggest both the compartmentalized release of NO and a greater diversity of cell types in placozoans than anticipated. NO receptor machinery includes both canonical and novel NIT-domain containing soluble guanylate cyclases as putative NO/nitrite/nitrate sensors. Thus, althoughTrichoplaxandHoilungiaexemplify the morphologically simplest free-living animals, the complexity of NO-cGMP-mediated signaling in Placozoa is greater to those in vertebrates. This situation illuminates multiple lineage-specific diversifications of NOSs and NO/nitrite/nitrate sensors from the common ancestor of Metazoa and the preservation of conservative NOS architecture from prokaryotic ancestors.