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The generality of transient compartmentalization and its associated error thresholds
Alex Blokhuis, Philippe Nghe , Luca Peliti , David Lacoste
J Theor Biol . - 487 110110 - doi: 10.1016/j.jtbi.2019.110110 - 2020
Can prelife proceed without cell division? A recently proposed mechanism suggests that transient compartmentalization could have preceded cell division in prebiotic scenarios. Here, we study transient compartmentalization dynamics in the presence of mutations and noise in replication, as both can be detrimental the survival of compartments. Our study comprises situations where compartments contain uncoupled autocatalytic reactions feeding on a common resource, and systems based on RNA molecules copied by replicases, following a recent experimental study. Using the theory of branching processes, we show analytically that two regimes are possible. In the diffusion-limited regime, replication is asynchronous which leads to a large variability in the composition of compartments. In contrast, in a replication-limited regime, the growth is synchronous and thus the compositional variability is low. Typically, simple autocatalysts are in the former regime, while polymeric replicators can access the latter. For deterministic growth dynamics, we introduce mutations that turn functional replicators into parasites. We derive the phase boundary separating coexistence or parasite dominance as a function of relative growth, inoculation size and mutation rate. We show that transient compartmentalization allows coexistence beyond the classical error threshold, above which the parasite dominates. Our findings invite to revisit major prebiotic transitions, notably the transitions towards cooperation, complex polymers and cell division.
Flux, toxicity and protein expression costs shape genetic interaction in a metabolic pathways
Gabrielle Woronoff, Philippe Nghe, Jean Baudry, Laurent Boitard, Erez Bra
Science Advances - 6 23 - DOI: 10.1126/sciadv.abb2236 - 2020
Our ability to predict the impact of mutations on traits relevant for disease and evolution remains severely limited by the dependence of their effects on the genetic background and environment. Even when molecular interactions between genes are known, it is unclear how these translate to organism-level interactions between alleles. We therefore characterized the interplay of genetic and environmental dependencies in determining fitness by quantifying ~4000 fitness interactions between expression variants of two metabolic genes, starting from various environmentally modulated expression levels. We detect a remarkable variety of interactions dependent on initial expression levels and demonstrate that they can be quantitatively explained by a mechanistic model accounting for catabolic flux, metabolite toxicity, and expression costs. Complex fitness interactions between mutations can therefore be predicted simply from their simultaneous impact on a few connected molecular phenotypes.

Meta population structure and the evolutionary transition to multicellularity
Caroline J. Rose Katrin Hammerschmidt Yuriy Pichugin Paul B. Rainey
First published - 23(9) 1380-1390 - - 2020
The evolutionary transition to multicellularity has occurred on numerous occasions, but transitions to complex life forms are rare. Here, using experimental bacterial populations as proxies for nascent multicellular organisms, we manipulate ecological factors shaping the evolution of groups. Groups were propagated under regimes requiring reproduction via a life cycle replete with developmental and dispersal (propagule) phases, but in one treatment lineages never mixed, whereas in a second treatment, cells from different lineages experienced intense competition during the dispersal phase. The latter treatment favoured traits promoting cell growth at the expense of traits underlying group fitness – a finding that is supported by results from a mathematical model. Our results show that the transition to multicellularity benefits from ecological conditions that maintain discreteness not just of the group (soma) phase, but also of the dispersal (germline) phase.

Genotypic and phenotypic analyses reveal distinct population structures and ecotypes for sugar beet‐associated Pseudomonas in Oxford and Auckland
Xue‐Xian Zhang,corresponding author, Stephen R. Ritchie, Hao Chang, Dawn L. Arnold, Robert W. Jackson, and Paul B. Rainey
Ecol Evol - 10(12) 5963–5975 - doi: 10.1002/ece3.6334 - 2020
Fluorescent pseudomonads represent one of the largest groups of bacteria inhabiting the surfaces of plants, but their genetic composition in planta is poorly understood. Here, we examined the population structure and diversity of fluorescent pseudomonads isolated from sugar beet grown at two geographic locations (Oxford, United Kingdom and Auckland, New Zealand). To seek evidence for niche adaptation, bacteria were sampled from three types of leaves (immature, mature, and senescent) and then characterized using a combination of genotypic and phenotypic analysis. We first performed multilocus sequence analysis (MLSA) of three housekeeping genes (gapA, gltA, and acnB) in a total of 152 isolates (96 from Oxford, 56 from Auckland). The concatenated sequences were grouped into 81 sequence types and 22 distinct operational taxonomic units (OTUs). Significant levels of recombination were detected, particularly for the Oxford isolates (rate of recombination to mutation (r/m) = 5.23 for the whole population). Subsequent ancestral analysis performed in STRUCTURE found evidence of six ancestral populations, and their distributions significantly differed between Oxford and Auckland. Next, their ability to grow on 95 carbon sources was assessed using the Biolog™ GN2 microtiter plates. A distance matrix was generated from the raw growth data (A 660) and subjected to multidimensional scaling (MDS) analysis. There was a significant correlation between substrate utilization profiles and MLSA genotypes. Both phenotypic and genotypic analyses indicated presence of a geographic structure for strains from Oxford and Auckland. Significant differences were also detected for MLSA genotypes between strains isolated from immature versus mature/senescent leaves. The fluorescent pseudomonads thus showed an ecotypic population structure, suggestive of adaptation to both geographic conditions and local plant niches.

My Science Work - - - 2020
The present invention relates to a method for manipulating the evolution of collectives of self-replicating entities and/or variation between collectives of self-replicating entities, in a high throughput droplet milli-fluidic system.
Experimental manipulation of selfish genetic elements links genes to microbial community function
Steven D. Quistad, Guilhem Doulcier and Paul B. Rainey
Philosophical Transactions of the Royal Society - - - 2020
Microbial communities underpin the Earth's biological and geochemical processes, but their complexity hampers understanding. Motivated by the challenge of diversity and the need to forge ways of capturing dynamical behaviour connecting genes to function, biologically independent experimental communities comprising hundreds of microbial genera were established from garden compost and propagated on nitrogen-limited minimal medium with cellulose (paper) as sole carbon source. After 1 year of bi-weekly transfer, communities retained hundreds of genera. To connect genes to function, we used a simple experimental manipulation that involved the periodic collection of selfish genetic elements (SGEs) from separate communities, followed by pooling and redistribution across communities. The treatment was predicted to promote amplification and dissemination of SGEs and thus horizontal gene transfer. Confirmation came from comparative metagenomics, which showed the substantive movement of ecologically significant genes whose dynamic across space and time could be followed. Enrichment of genes implicated in nitrogen metabolism, and particularly ammonification, prompted biochemical assays that revealed a measurable impact on community function. Our simple experimental strategy offers a conceptually new approach for unravelling dynamical processes affecting microbial community function.

Toward a dynamical understanding of microbial communities
Paul B. Rainey and Steven D. Quistad
Philosophical Transactions of the Royal Society - - - 2020
The challenge of moving beyond descriptions of microbial community composition to the point where understanding underlying eco-evolutionary dynamics emerges is daunting. While it is tempting to simplify through use of model communities composed of a small number of types, there is a risk that such strategies fail to capture processes that might be specific and intrinsic to complexity of the community itself. Here, we describe approaches that embrace this complexity and show that, in combination with metagenomic strategies, dynamical insight is increasingly possible. Arising from these studies is mounting evidence of rapid eco-evolutionary change among lineages and a sense that processes, particularly those mediated by horizontal gene transfer, not only are integral to system function, but are central to long-term persistence. That such dynamic, systems-level insight is now possible, means that the study and manipulation of microbial communities can move to new levels of inquiry.

Eco-evolutionary dynamics of nested Darwinian populations and the emergence of community-level heredity
Guilhem Doulcier, Amaury Lambert, Silvia De Monte, Paul B Rainey
EcologyEvolutionary Biology - - DOI: 10.7554/eLife.53433 - 2020
Interactions among microbial cells can generate new chemistries and functions, but exploitation requires establishment of communities that reliably recapitulate community-level phenotypes. Using mechanistic mathematical models, we show how simple manipulations to population structure can exogenously impose Darwinian-like properties on communities. Such scaffolding causes communities to participate directly in the process of evolution by natural selection and drives the evolution of cell-level interactions to the point where, despite underlying stochasticity, derived communities give rise to offspring communities that faithfully re-establish parental phenotype. The mechanism is akin to a developmental process (developmental correction) that arises from density-dependent interactions among cells. Knowledge of ecological factors affecting evolution of developmental correction has implications for understanding the evolutionary origin of major egalitarian transitions, symbioses, and for top-down engineering of microbial communities.

Ecological scaffolding and the evolution of individuality
Andrew J. Black, Pierrick Bourrat & Paul B. Rainey
Nature Ecology & Evolution - 4 426–436 - - 2020
Evolutionary transitions in individuality are central to the emergence of biological complexity. Recent experiments provide glimpses of processes underpinning the transition from single cells to multicellular life and draw attention to the critical role of ecology. Here, we emphasize this ecological dimension and argue that its current absence from theoretical frameworks hampers development of general explanatory solutions. Using mechanistic mathematical models, we show how a minimal ecological structure comprising patchily distributed resources and between-patch dispersal can scaffold Darwinian-like properties on collectives of cells. This scaffolding causes cells to participate directly in the process of evolution by natural selection as if they were members of multicellular collectives, with collectives participating in a death–birth process arising from the interplay between the timing of dispersal events and the rate of resource use by cells. When this timescale is sufficiently long and new collectives are founded by single cells, collectives experience conditions that favour evolution of a reproductive division of labour. Together our simple model makes explicit key events in the major evolutionary transition to multicellularity. It also makes predictions concerning the life history of certain pathogens and serves as an ecological recipe for experimental realization of evolutionary transitions.

Ultrafast photomechanical transduction through thermophoretic implosion
N. Kavokine, S. Zou, R. Liu, H. Zhong, A. Nigues, B. Zou and L. Bocquet
Nature Communications - 11(1) 50 - - 2020
Since the historical experiments of Crookes, the direct manipulation of matter by light has been both a challenge and a source of scientific debate. Here we show that laser illumination allows to displace a vial of nanoparticle solution over centimetre-scale distances. Cantilever-based force measurements show that the movement is due to millisecond-long force spikes, which are synchronised with a sound emission. We observe that the nanoparticles undergo negative thermophoresis, and ultrafast imaging reveals that the force spikes are followed by the explosive growth of a bubble in the solution. We propose a mechanism accounting for the propulsion based on a thermophoretic instability of the nanoparticle cloud, analogous to the Jeans’s instability that occurs in gravitational systems. Our experiments demonstrate a new type of laser propulsion and a remarkably violent actuation of soft matter, reminiscent of the strategy used by certain plants to propel their spores.


- For any publication having received the support of the IPGG (presence in the IPGG premises, use of the IPGG technological platform, collaboration between IPGG teams, linked to an IPGG doctoral or postdoctoral grant, or use of the common spaces), you must indicate the following sentence : "This work has received the support of "Institut Pierre-Gilles de Gennes" (laboratoire d'excellence, "Investissements d'avenir" program ANR-10-IDEX-0001-02 PSL and ANR-10-LABX-31.) ".

- For any publication of results obtained through the use of equipment purchased by the Equipex IPGG, you must add the following coding: "ANR-10-EQPX-34".

579 publications.