Maxime ARQUE

PhD project : Pangenome dynamics and functional sharing within aquatic microbial communities
 

PhD project summary : Aquatic bacterial populations evolve in ecosystems characterized by nutrient limitations, imposing strong selective pressures. To adapt to these oligotrophic conditions (i.e., environments poor in mineral nutrients), bacteria have developed specific evolutionary strategies, notably involving a drastic reduction in cell size, a smaller genome (usually under 2 Mb), and simplified metabolic pathways. This phenomenon frequently leads to auxotrophy (i.e., the inability to synthesize) for various metabolites, making these organisms dependent on external sources, especially other members of their microbial communities, for supplying essential compounds necessary for their survival. This metabolic dependency, though seemingly restrictive, is actually an advantageous adaptive strategy aligned with the "Black Queen Hypothesis" (BQH). According to this hypothesis, losing costly biological functions enables organisms to decrease their energy and metabolic expenditure, thereby conferring a competitive advantage within complex microbial communities and promoting their long-term evolutionary success (fig. 1). Moreover, these organisms possess open pangenomes characterized by significant genetic diversity arising from a dynamic accessory genome. Studying this accessory genome helps elucidate the adaptive potential of bacterial populations and the evolutionary mechanisms influenced by various biotic and abiotic factors. This approach notably facilitates a better understanding of the processes involved in genomic reduction and the coexistence of diverse ecotypes in these specific environments.

In this context, this doctoral project aims to characterize metabolic dependencies within aquatic microbial communities and analyze the dynamics of accessory genomes to identify mechanisms underlying the emergence or loss of biological functions. This will be conducted using a bioinformatics approach based on existing genomic and metagenomic data analysis.


Keywords: Aquatic ecosystems, Microbial communities, Black Queen Hypothesis, Auxotrophy, Pangenome

Figure 1 : The Black Queen Hypothesis is an evolutionary framework suggesting that certain species can lose energetically expensive biological functions when these functions are reliably provided by other members of their community (Morris, 2015). In this scenario, gene loss is not inherently detrimental ;  instead, it can represent an adaptive strategy to conserve energy, provided the lost function remains essential to survival and is maintained at the community level (Hesse & O’Brien, 2024). This sets the stage for a form of interdependence, where some organisms (often unintentionally) act as altruists, supporting the survival of others while streamlining their own genomes.

For example, consider two distinct bacterial species that both initially possess genes encoding detoxification enzymes (an energetically costly trait). Through co-evolution and selective pressure, a division of labor may emerge. If one species begins to overproduce these enzymes, the other may benefit by shedding the corresponding genes. This loss not only reduces its genomic and metabolic burden but also enhances its fitness by allowing it to exploit a communal resource without bearing the production cost. In such systems, gene loss becomes a form of evolutionary economization, tightly coupled to community structure and function.