Embryo-like features in developing Bacillus subtilis biofilms

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 likely 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 ontogeny of growing Bacillus subtilis biofilms recapitulates phylogeny at the expression level. Using finely resolved transcriptome and proteome profiles, we found that biofilm ontogeny correlates with the evolutionary measures. Early-stage biofilms expressed older and more conserved genes, while later-stage biofilms progressively used evolutionary younger and more diverged genes. Molecular and morphological signatures also revealed that biofilm growth is highly regulated and organized into discrete ontogenetic stages, similar to those of eukaryotic embryos. In conjunction 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.