Embryo-like features in developingBacillus subtilisbiofilms

Abstract

34Correspondence between evolution and development has been discussed for more than 35 two centuries 1 . Recent work reveals that phylogeny-ontogeny correlations are indeed 36 present in developmental transcriptomes of eukaryotic clades with complex 37 multicellularity 2-10 . Nevertheless, it has been largely ignored that the pervasive presence 38 of phylogeny-ontogeny correlations is a hallmark of development in eukaryotes 6,10-12 . This 39 perspective opens a possibility to look for similar parallelisms in biological settings where 40 developmental logic and multicellular complexity are more obscure [13][14][15][16] . For instance, it 41 has been increasingly recognized that multicellular behaviour underlies biofilm formation 42 in bacteria 13,14,[17][18][19] . However, it remains unclear whether bacterial biofilm growth shares 43 some basic principles with development in complex eukaryotes [14][15][16]18,20 . Here we show that 44 the ontogeny of growing Bacillus subtilis biofilms recapitulates phylogeny at the 45 expression level. Using time-resolved transcriptome and proteome profiles, we found that 46 biofilm ontogeny correlates with the evolutionary measures, in a way that evolutionary 47 younger and more diverged genes were increasingly expressed towards later timepoints 48 of biofilm growth. Molecular and morphological signatures also revealed that biofilm 49 growth is highly regulated and organized into discrete ontogenetic stages, analogous to 50 those of eukaryotic embryos 11,21 . Together, this suggests that biofilm formation in Bacillus 51 is a bona fide developmental process comparable to organismal development in animals, 52 plants and fungi. Given that most cells on Earth reside in the form of biofilms 22 and that 53 biofilms represent the oldest known fossils 23 , we anticipate that the widely-adopted vision 54 of the first life as a single-cell and free-living organism needs rethinking. 55 56 Multicellular behaviour is wide-spread in bacteria and it was proposed that they should be 57 considered multicellular organisms 13 . However, this idea has not been generally adopted likely 58 3 due to the widespread laboratory use of domesticated bacterial models selected against 59 multicellular behaviours, the long tradition of viewing early diverging groups as simple, and 60 the lack of evidence for system-level commonalities between bacteria and multicellular 61 eukaryotes 15,16,18,24 . Recently developed phylo-transcriptomic tools for tracking evolutionary 62 signatures in animal development 2-4 were also successfully applied in the analysis of 63 developmental processes in plants and fungi 5,6,10 . Although development evolved 64 independently in these three major branches of eukaryotic diversity 12 , their ontogenies showed 65 similar phylogeny-ontogeny correlations indicating that possibly all eukaryotic developmental 66 programs have an evolutionary imprint. Transferability of the phylo-transcriptomic tools across 67 clades and likely universal patterns of phylogeny-ontogeny correlations in e...

Somatic embryogenesis of grapevine (Vitis vinifera) expresses a transcriptomic hourglass

“…To get further insights into expression dynamics along the SE developmental trajectory, we performed principal component analysis (PCA) which revealed a time-resolved profile that follows the developmental progression of somatic embryogenesis and shows its punctuated organization (Figure 2). The general organization of this PCA pattern in SE is similar to those previously recovered in bacterial biofilm development (Futo et al 2021). This suggests that these developmental processes, although analogous, are governed by the common basic principles.…”

“…This suggests that these developmental processes, although analogous, are governed by the common basic principles. Similar to bacterial biofilm development (Futo et al 2021), biological replicates per developmental stage generally clustered together (Figure 2). The only stage that showed increased distortion in expression between replicates is cotyledonary stage 1 (C1).…”

“…Curiously, we recently found that similar regularities are also present in the development of bacterial biofilms; a process that mimics embryogenesis of multicellular eukaryotes (Futo et al 2021). However, an hourglass-shaped correlation between ontogeny and phylogeny is a unique feature of multicellular eukaryotes.…”

“…We matched the obtained expression values to gene-related evolutionary and functional information to explore the correspondence between ontogeny and phylogeny along the SE developmental trajectory. To achieve this, we applied phylostratigraphic and phylotranscriptomic methods which are very powerful in extracting macroevolutionary information from genomic and developmental data (Domazet-Lošo et al 2007, Domazet-Lošo and Tautz 2010a, Domazet-Lošo and Tautz 2010b, Quint et al 2012, Domazet-Lošo et al 2017, Drost et al 2018, Futo et al 2021, Domazet-Lošo et al 2024).…”

Biofilm Dispersal for Spore Release in Bacillus subtilis

“…Additionally, it has been proposed that during biofilm colony maturation, the evolutionary younger and more diverged genes are increasingly expressed toward later timepoints of colony development (16).…”