Yashraj Chavhan

I have a new paper on the evolution of macroscopic multicellularity:

 

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The first paper from my ongoing postdoc with Dr. Peter Lind is now published! Click here for the full text. I had made the initial discovery in 2014 and had been waiting for the right opportunity to test my ideas and develop this line of work, which I got in December 2021. This is my first publication as a corresponding author.

 

Here's a brief summary of this study:

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The evolutionary transition from unicellular organisms to multicellularity opened key gateways towards innovation and complexity in the history of life. While experimental evolution is an important tool to study this fundamental transition, it suffers from two blind spots: (1) Although multicellularity first evolved in bacteria, the existing experimental evolution research deals primarily with eukaryotes. (2) It focuses on mutationally driven (and not environmentally induced) phenotypes. In the second year of my PhD at IISER Pune (2014), I observed something that had the potential to fix these limitations. Specifically, I observed that highly saline liquid environments make the bacterium Escherichia coli grow as large elongated multicellular clusters, not just as planktonic cells:

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After starting my postdoctoral work in Sweden, I starting developing this line of work (originally as a side project). I established that both Gram -ve & Gram +ve bacteria exhibit phenotypically plastic cell clustering. Under high salinity, they grow as elongated clusters (not as planktonic cells). But under habitual salinity, the clusters disintegrate and grow planktonically. This is how the plastic phenototype looks in wildtype E. coli:

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Although such pehnotypically plastic cell clustering is widespread among bacteria, it is not a physically inevitable outcome of bacterial growth under high salinity (the bacterium Serratia marcescens does not do it):

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This made me think about the evolvability of such phenotypically plastic bacterial clustering. So, in order to test if the such clustering was itself an evolvable biological phenomenon, I conducted experimental evolution with E. coli and found that ancestrally plastic cell clustering can be genetically assimilated (its expression can be made constitutive)! The evolved bacteria obligately grow as macroscopic multicellular clusters, even without environmental induction:

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I also found that highly parallel mutations in genes linked to cell wall assembly formed the genomic basis of assimilated multicellularity:

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What's even more interesting is that mraY (an essential gene linked to cell wall assembly, specifically to peptidoglycan biosynthesis) mutated in 70% of the evolved clones that we sequenced. It was fascinating that each and every one of the several distinct mutations in the transmembrane protein MraY was located in its periplasmic region (away from its cytoplasmic enzymatic active site):

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I also established that the wildtype E. coli also showed cell shape plasticity: rod-shaped cells under habitual salinity, but small spherical cells under high salinity. Surprisingly, the ancestral cell perimeter reaction norm reversed upon evolution:

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A single mutation could genetically assimilate multicellularity by modulating plasticity at multiple levels of organization:

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I observed opposite evolutionary journeys of plasticity across distinct levels of biological organization: At the level of cell collectives, the induced phenotype (cell clustering) got assimilated. In contrast, at the level of cells, the uninduced phenotype (non-spherical cells) did so:

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This means that the ancestral multilevel plasticity is an unreliable indicator of how multilevel phenotypes will evolve. This was a major insight for me!

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I also found an important result in the role played by plasticity in guiding evolution: The biochemical basis of the genetically assimilated (uninduced) clustering was distinct from that of induced clustering:

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This shows that the genetic assimilation of a higher-level phenotype can be brought about by the expression of contrasting lower-level phenotypes.

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The evolved clones can successfully undergo a life cycle in which a macroscopic multicellular cluster can spontaneously give rise to another macroscopic cluster via the growth of small propagules upon accessing fresh nutrients:

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Taken together, we show that phenotypic plasticity can facilitate a major transition in evolution and can prime bacteria for evolving undifferentiated macroscopic multicellularity.

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I cannot thank Dr. Peter Lind enough for giving me complete freedom to design and execute risky experiments. I am truly grateful to both Dr. Peter Lind and Prof. Sutirth Dey for supporting my ideas!

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The graphics and videos in this summary have been adapted (to aid navigation and provide simplicity) under a Creative Commons Attribution 4.0 International License form the original graphics and videos presented in our paper (https://doi.org/10.1038/s41467-023-39320-9); the authors (myself, Sutirth Dey, and Peter A. Lind) hold the original copyright.