Embryo-Like Features in Developing Bacillus subtilis Biofilms
Journal article, 2021

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.

phylogeny-ontogeny correlations

proteome

biofilms

evo-devo

Bacillus

transcriptome

Author

Momir Futo

Ruđer Bošković Institute

Luka Opasic

Ruđer Bošković Institute

Max Planck Society

Sara Koska

Ruđer Bošković Institute

Nina Corak

Ruđer Bošković Institute

Tin Siroki

University of Zagreb

Vaishnavi Ravikumar

Technical University of Denmark (DTU)

Annika Thorsell

University of Gothenburg

Masa Lenuzzi

Ruđer Bošković Institute

Max Planck Society

Domagoj Kifer

University of Zagreb

Mirjana Domazet-Loso

University of Zagreb

Kristian Vlahovicek

University of Skövde

University of Zagreb

Ivan Mijakovic

Chalmers, Biology and Biological Engineering, Systems and Synthetic Biology

Tomislav Domazet-Loso

Ruđer Bošković Institute

Catholic University of Croatia

Molecular Biology and Evolution

0737-4038 (ISSN) 1537-1719 (eISSN)

Vol. 38 1 31-47

Subject Categories

Botany

Developmental Biology

Medical Biotechnology (with a focus on Cell Biology (including Stem Cell Biology), Molecular Biology, Microbiology, Biochemistry or Biopharmacy)

DOI

10.1093/molbev/msaa217

PubMed

32871001

More information

Latest update

3/5/2021 4