Social behaviours by <i>Bacillus subtilis</i>: quorum sensing, kin discrimination and beyond

Kalamara, Margarita; Špacapan, Mihael; Mandić-Mulec, Ines; Stanley‐Wall, Nicola R.

doi:10.1111/mmi.14127

Cited by 134 publications

(124 citation statements)

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“…This is in line with evidence 326 demonstrating that exoproteases control both the production and degradation of the quorum sensing 327 signalling molecule ComX ). An accumulation of quorum sensing peptides in the 328 biofilm microenvironment may have a global impact on the physiology of the KO8 strain due to an 329 alteration in cell signalling pathways (Kalamara et al, 2018, Miller & Bassler, 2001. 330…”

Section: Discussion: 286mentioning

confidence: 99%

The majority of the matrix protein TapA is dispensable for biofilm formation byBacillus subtilis

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Arnaouteli

Sukhodub

et al. 2019

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20 21 extracellular proteases, we show that proteolytic cleavage by these enzymes is not a prerequisite for TapA 33 function. It remains unknown why TapA is synthesized at a full length of 253 amino acids when the first 34 57 are sufficient for biofilm structuring, but the findings do not exclude the core conserved region of TapA 35 having a second role beyond that of structuring the B. subtilis biofilm. 36 37

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Section: Discussion: 286mentioning

confidence: 99%

The majority of the matrix protein TapA is dispensable for biofilm formation byBacillus subtilis

Earl

Arnaouteli

Sukhodub

et al. 2019

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“…This perspective opens a possibility to look for similar parallelisms in biological settings where developmental logic and multicellular complexity are more obscure 13–16 . For instance, it has been increasingly recognized that multicellular behaviour underlies biofilm formation in bacteria 13, 14, 17–19 . However, it remains unclear whether bacterial biofilm growth shares some basic principles with development in complex eukaryotes 14–16, 18, 20 .…”

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Embryo-like features in developingBacillus subtilisbiofilms

Futo

Opasic

Koska

et al. 2020

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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...

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“…B. subtilis is a soil dwelling bacterium with a diverse social life that includes quorum sensingregulated interactions 1 . These interactions result in bacterial equivalent of sex, and subsequently have a profound influence on bacterial evolution 2 .…”

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Kin discrimination promotes horizontal gene transfer between unrelated strains inBacillus subtilis

Štefanič

Belcijan

Kraigher

et al. 2019

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authors contributed equally to this work.B. subtilis is a soil dwelling bacterium with a diverse social life that includes quorum sensingregulated interactions 1 . These interactions result in bacterial equivalent of sex, and subsequently have a profound influence on bacterial evolution 2 . Sexual isolation in B. subtilis predicts for more frequent uptake of DNA isolated from closely related strains 3-5 , but DNA exchange between two interacting B. subtilis strains has never been addressed previously. Recently we discovered kin discrimination among highly related strains of B. subtilis, where less related strains showed antagonistic behaviour towards each other in the form of killing 6 . Here we show that antagonistic interactions between two less closely related B. subtilis strains result in increased recombination, which is in contrast to current dogma. We demonstrate that the induction of competence between non-kin strains is responsible for the observed elevated DNA uptake, which, through increased genetic variation, can increase the rate of adaptation as demonstrated here by the successful exploitation of a novel adaptive zone by a recombinant strain. Our results demonstrate an important evolutionary mechanism of ''promiscuous but safe sex'': a type of bacterial cell-contact dependent DNA exchange that could promote diversification of conspecifics and exclude nonspecific and potentially risky DNA of other species. Our findings could help understand the vast diversity of B. subtilis species at the genomic level despite existing mechanisms limiting lessrelated DNA integration during transformation. It is possible that this (or similar) mechanism could be accountable for the diversification of many other bacterial species capable of natural transformation.

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Social behaviours by Bacillus subtilis: quorum sensing, kin discrimination and beyond

Cited by 134 publications

References 145 publications

The majority of the matrix protein TapA is dispensable for biofilm formation byBacillus subtilis

The majority of the matrix protein TapA is dispensable for biofilm formation byBacillus subtilis

Embryo-like features in developingBacillus subtilisbiofilms

Kin discrimination promotes horizontal gene transfer between unrelated strains inBacillus subtilis

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