Pérez Gallego Ruth, von Meijenfeldt F A Bastiaan, Bale Nicole J, Sinninghe Damsté Jaap S, Villanueva Laura
Department of Marine Microbiology and Biogeochemistry, Royal Netherlands Institute for Sea Research (NIOZ), Den Burg 1790 AB, The Netherlands.
Department of Earth Sciences, Faculty of Geosciences, Utrecht University, Utrecht 3508 TA, The Netherlands.
Proc Natl Acad Sci U S A. 2025 Feb 4;122(5):e2413972122. doi: 10.1073/pnas.2413972122. Epub 2025 Jan 27.
Heterocytes, specialized cells for nitrogen fixation in cyanobacteria, are surrounded by heterocyte glycolipids (HGs), which contribute to protection of the nitrogenase enzyme from oxygen. Diverse HGs preserve in the sediment and have been widely used as evidence of past nitrogen fixation, and structural variation has been suggested to preserve taxonomic information and reflect paleoenvironmental conditions. Here, by comprehensive HG identification and screening of HG biosynthetic gene clusters throughout cyanobacteria, we reconstruct the convergent evolutionary history of HG structure, in which different clades produce the same HGs. We find that rudimentary HG biosynthetic machinery was already present in cyanobacteria before the emergence of heterocytes for functions unrelated to nitrogen fixation and identify HG analogs produced by specific and distantly related nonheterocytous cyanobacteria. These structurally less complex molecules represent precursors of HGs, suggesting that HGs arose after a genomic reorganization and expansion of ancestral biosynthetic machinery, enabling the rise of cyanobacterial heterocytes in an increasingly oxygenated atmosphere. Our results open a chapter in the potential use of diagenetic products of HGs and HG analogs as fossils for reconstructing the evolution of multicellularity and division of labor in cyanobacteria.
异形胞是蓝细菌中用于固氮的特化细胞，被异形胞糖脂（HG）所包围，这些糖脂有助于保护固氮酶免受氧气影响。多种HG保存在沉积物中，并被广泛用作过去固氮作用的证据，而且有人提出其结构变异能保留分类信息并反映古环境条件。在此，通过对整个蓝细菌进行全面的HG鉴定和HG生物合成基因簇筛选，我们重建了HG结构的趋同进化史，其中不同进化枝产生相同的HG。我们发现，在异形胞出现之前，蓝细菌中就已存在基本的HG生物合成机制，其功能与固氮无关，并且我们鉴定出了由特定且亲缘关系较远的非异形胞蓝细菌产生的HG类似物。这些结构上不太复杂的分子代表了HG的前体，这表明HG是在祖先生物合成机制发生基因组重组和扩展之后出现的，从而使得蓝细菌异形胞能够在日益氧化的大气中兴起。我们的研究结果开启了一个新篇章，即有可能利用HG及其类似物的成岩产物作为化石来重建蓝细菌中多细胞性和分工的进化过程。
