Institute of Ecological Science, Guangzhou Key Laboratory of Subtropical Biodiversity and Biomonitoring, Guangdong Provincial Key Laboratory of Biotechnology for Plant Development, School of Life Sciences, South China Normal University, Guangzhou, PR China.
State Key Laboratory of Biocontrol, Guangdong Key Laboratory of Plant Resources, School of Life Sciences, Sun Yat-sen University, Guangzhou, PR China.
Mol Biol Evol. 2022 Sep 1;39(9). doi: 10.1093/molbev/msac171.
Biological nitrogen fixation (BNF) by cyanobacteria is of significant importance for the Earth's biogeochemical nitrogen cycle but is restricted to a few genera that do not form monophyletic group. To explore the evolutionary trajectory of BNF and investigate the driving forces of its evolution, we analyze 650 cyanobacterial genomes and compile the database of diazotrophic cyanobacteria based on the presence of nitrogen fixation gene clusters (NFGCs). We report that 266 of 650 examined genomes are NFGC-carrying members, and these potentially diazotrophic cyanobacteria are unevenly distributed across the phylogeny of Cyanobacteria, that multiple independent losses shaped the scattered distribution. Among the diazotrophic cyanobacteria, two types of NFGC exist, with one being ancestral and abundant, which have descended from diazotrophic ancestors, and the other being anaerobe-like and sparse, possibly being acquired from anaerobic microbes through horizontal gene transfer. Interestingly, we illustrate that the origin of BNF in Cyanobacteria coincide with two major evolutionary events. One is the origin of multicellularity of cyanobacteria, and the other is concurrent genetic innovations with massive gene gains and expansions, implicating their key roles in triggering the evolutionary transition from nondiazotrophic to diazotrophic cyanobacteria. Additionally, we reveal that genes involved in accelerating respiratory electron transport (coxABC), anoxygenic photosynthetic electron transport (sqr), as well as anaerobic metabolisms (pfor, hemN, nrdG, adhE) are enriched in diazotrophic cyanobacteria, representing adaptive genetic signatures that underpin the diazotrophic lifestyle. Collectively, our study suggests that multicellularity, together with concurrent genetic adaptations contribute to the evolution of diazotrophic cyanobacteria.
蓝细菌的生物固氮（BNF）对地球的生物地球化学氮循环具有重要意义，但仅限于少数不形成单系群的属。为了探索 BNF 的进化轨迹并研究其进化的驱动力，我们分析了 650 个蓝细菌基因组，并根据固氮基因簇（NFGC）的存在编译了固氮蓝细菌数据库。我们报告说，在 650 个被检查的基因组中，有 266 个是 NFGC 携带成员，这些潜在的固氮蓝细菌在蓝细菌的系统发育中分布不均，多次独立的缺失导致了分散的分布。在固氮蓝细菌中，存在两种类型的 NFGC，一种是祖先进化且丰富的，它来自固氮祖先，另一种是类似厌氧的稀疏的，可能是通过水平基因转移从厌氧微生物中获得的。有趣的是，我们说明了 BNF 在蓝细菌中的起源与两个主要的进化事件同时发生。一个是蓝细菌多细胞化的起源，另一个是与大量基因获得和扩展相关的遗传创新，暗示它们在触发从非固氮到固氮蓝细菌的进化转变中起着关键作用。此外，我们还揭示了参与加速呼吸电子传递（coxABC）、缺氧光合作用电子传递（sqr）以及厌氧代谢（pfor、hemN、nrdG、adhE）的基因在固氮蓝细菌中富集，代表了支持固氮生活方式的适应性遗传特征。总的来说，我们的研究表明，多细胞性以及同时发生的遗传适应有助于固氮蓝细菌的进化。
