Abstract

Correspondence between evolution and development has been discussed for more than two centuries. Recent work reveals that phylogeny−ontogeny correlations are indeed present in developmental transcriptomes of eukaryotic clades with complex multicellularity. Nevertheless, it has been largely ignored that the pervasive presence of phylogeny−ontogeny correlations is a hallmark of development in eukaryotes. This perspective opens a possibility to look for similar parallelisms in biological settings where developmental logic and multicellular complexity are more obscure. For instance, it has been increasingly recognized that multicellular behavior underlies biofilm formation in bacteria. However, it remains unclear whether bacterial biofilm growth shares some basic principles with development in complex eukaryotes. Here we show that the ontogeny of growing Bacillus subtilis biofilms recapitulates phylogeny at the expression level. Using time-resolved transcriptome and proteome profiles, we found that biofilm ontogeny correlates with the evolutionary measures, in a way that evolutionary younger and more diverged genes were increasingly expressed toward later timepoints of biofilm growth. Molecular and morphological signatures also revealed that biofilm growth is highly regulated and organized into discrete ontogenetic stages, analogous to those of eukaryotic embryos. Together, this suggests that biofilm formation in Bacillus is a bona fide developmental process comparable to organismal development in animals, plants, and fungi. Given that most cells on Earth reside in the form of biofilms and that biofilms represent the oldest known fossils, we anticipate that the widely adopted vision of the first life as a single-cell and free-living organism needs rethinking.

中文翻译：

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枯草芽孢杆菌生物膜发育中的胚胎样特征。

摘要

两个多世纪以来，人们一直在讨论进化与发展之间的对应关系。最近的工作表明，系统发育-个体发育相关性确实存在于具有复杂多细胞性的真核进化枝的发育转录组中。然而，人们在很大程度上忽视了普遍存在的系统发育-个体发育相关性是真核生物发育的标志。这种观点为在发育逻辑和多细胞复杂性更加模糊的生物环境中寻找类似的并行性提供了可能性。例如，人们越来越认识到多细胞行为是细菌生物膜形成的基础。然而，目前尚不清楚细菌生物膜的生长是否与复杂真核生物的发育有一些共同的基本原理。在这里，我们表明生长的枯草芽孢杆菌生物膜的个体发育在表达水平上概括了系统发育。使用时间分辨转录组和蛋白质组图谱，我们发现生物膜个体发育与进化测量相关，在某种程度上，进化上更年轻和更分化的基因在生物膜生长的较晚时间点越来越多地表达。分子和形态学特征还表明，生物膜的生长受到高度调控，并组织成离散的个体发育阶段，类似于真核胚胎的阶段。总之，这表明芽孢杆菌中生物膜的形成是一个真正的发育过程，与动物、植物和真菌的有机体发育相当。鉴于地球上的大多数细胞以生物膜的形式存在，并且生物膜代表了已知最古老的化石，我们预计，广泛采用的第一个生命作为单细胞和自由生活的有机体的观点需要重新思考。