Moya-Beltrán Ana, Rojas-Villalobos Camila, Díaz Mauricio, Guiliani Nicolás, Quatrini Raquel, Castro Matías
Microbial Ecophysiology Laboratory, Fundación Ciencia & Vida, Santiago, Chile.
Facultad de Ciencias de la Vida, Universidad Andrés Bello, Santiago, Chile.
Front Microbiol. 2019 Mar 7;10:381. doi: 10.3389/fmicb.2019.00381. eCollection 2019.
Cyclic and linear nucleotides are key elements of the signal transduction networks linking perception of the environment to specific cellular behavior of prokaryotes. These molecular mechanisms are particularly important in bacteria exposed to different, and frequently simultaneous, types of extreme conditions. This is the case in acidithiobacilli, a group of extremophilic bacteria thriving in highly acidic biotopes, that must also cope with significant variations in temperature, osmotic potentials and concentrations of various transition metals and metalloids. Environmental cues sensed by bacteria are transduced into differential levels of nucleotides acting as intracellular second messengers, promoting the activation or inhibition of target components and eliciting different output phenotypes. Cyclic (c) di-GMP, one of the most common bacterial second messengers, plays a key role in lifestyle changes in many bacteria, including acidithiobacilli. The presence of functional c-di-GMP-dependent signal transduction pathways in representative strains of the best-known linages of this species complex has been reported. However, a comprehensive panorama of the c-di-GMP modulated networks, the cognate input signals and output responses, are still missing for this group of extremophiles. Moreover, little fundamental understanding has been gathered for other nucleotides acting as second messengers. Taking advantage of the increasing number of sequenced genomes of the taxon, here we address the challenge of disentangling the nucleotide-driven signal transduction pathways in this group of polyextremophiles using comparative genomic tools and strategies. Results indicate that the acidithiobacilli possess all the genetic elements required to establish functional transduction pathways based in three different nucleotide-second messengers: (p)ppGpp, cyclic AMP (cAMP), and c-di-GMP. The elements related with the metabolism and transduction of (p)ppGpp and cAMP appear highly conserved, integrating signals related with nutrient starvation and polyphosphate metabolism, respectively. In contrast, c-di-GMP networks appear diverse and complex, differing both at the species and strain levels. Molecular elements of c-di-GMP metabolism and transduction were mostly found scattered along the flexible genome of the acidithiobacilli, allowing the identification of probable control modules that could be critical for substrate colonization, biofilm development and intercellular interactions. These may ultimately convey increased endurance to environmental stress and increased potential for gene sharing and adaptation to changing conditions.
环核苷酸和线性核苷酸是原核生物中连接环境感知与特定细胞行为的信号转导网络的关键要素。这些分子机制在暴露于不同且常常同时存在的极端条件类型的细菌中尤为重要。嗜酸氧化硫硫杆菌就是这样的情况，这是一群在高酸性生物群落中繁衍生息的嗜极细菌，它们还必须应对温度、渗透势以及各种过渡金属和类金属浓度的显著变化。细菌感知到的环境信号被转化为作为细胞内第二信使的不同水平的核苷酸，促进靶标成分的激活或抑制，并引发不同的输出表型。环（c）二鸟苷单磷酸（c-di-GMP）是最常见的细菌第二信使之一，在包括嗜酸氧化硫硫杆菌在内的许多细菌的生活方式转变中起关键作用。据报道，在该物种复合体最著名谱系的代表性菌株中存在功能性的依赖c-di-GMP的信号转导途径。然而，对于这组嗜极菌，c-di-GMP调节网络、相关输入信号和输出反应的全面全景仍然缺失。此外，对于作为第二信使的其他核苷酸，人们几乎没有获得基本的了解。利用该分类群中测序基因组数量的增加，我们在此利用比较基因组工具和策略应对解开这组多嗜极菌中核苷酸驱动的信号转导途径这一挑战。结果表明，嗜酸氧化硫硫杆菌拥有基于三种不同核苷酸第二信使建立功能性转导途径所需的所有遗传元件：（p）ppGpp、环磷酸腺苷（cAMP）和c-di-GMP。与（p）ppGpp和cAMP的代谢及转导相关的元件显得高度保守，分别整合了与营养饥饿和多磷酸盐代谢相关的信号。相比之下，c-di-GMP网络显得多样且复杂，在物种和菌株水平上都有所不同。c-di-GMP代谢和转导的分子元件大多沿着嗜酸氧化硫硫杆菌的灵活基因组分散分布，这使得能够识别可能对底物定殖、生物膜形成和细胞间相互作用至关重要的控制模块。这些最终可能传达对环境压力更强的耐受性以及基因共享和适应变化条件的更大潜力。
