Periodic Reporting for period 1 - ARAMIS (Adaptive Radiation in Aquatic MIcrobial Species)
Période du rapport: 2021-03-01 au 2023-02-28
Understanding the ecological processes affecting freshwater sources is of capital importance in order to secure a sufficient supply of high quality water. Microorganisms hold a key position in freshwater ecosystems due to their ability to cycle and transform most bioactive compounds, but also in their trophic coupling to eukaryote predators. Both processes have a great impact on water quality, which has fueled a renewed interest in elucidating the spatio-temporal dynamics of the involved microbial taxa.
Our ability to study microbial communities has steadily increased over the last decades. Recently, we have become capable of distinguishing between closely related bacteria, even those belonging to the same species. This has revealed that freshwater bacterial species are actually composed of several subspecies or ecotypes, each with different optimum growth conditions, which replace one another as the environment changes. This intra-species diversity ensures that the species remains present under different environmental conditions, presumably enhancing the stability of the whole ecosystem.
The nature of this intra-species diversity is however unclear. Microbial species are difficult to define, as microorganisms can exchange genetic material via horizontal gene transfer. Because of this, some adaptive genes may not be exclusive of a single bacteria, but instead distributed across a common gene pool. Thus, each ecotype might not actually be a single entity, but a myriad of different bacteria all carrying the adaptive gene while differing otherwise. How are microbial species organized internally? What are the drivers of their diversification? Answering these questions could have large implications in the way we understand microbial species and ecosystems.
The ARAMIS project (Adaptive Radiation in Aquatic MIcrobial Species) aims to advance our understanding on the nature of microbial species, their evolution, and the ecological consequences of intra-species diversity. To achieve this, we collected genomic and metagenomic data from microbial communities in several lakes, and analyzed the internal dynamics of several cosmopolitan freshwater bacterial species through space, time and environmental gradients. We concluded that for some species ecotypes are indeed fuzzy, and that the drivers of intra-species diversification can operate at the gene level rather than the genome level. Furthermore, while this study focused on selection as the driver of intra-species diversification, we found an unexpected signal of dispersal limitation when comparing populations of the same species inhabiting geographically distant lakes.
Our ability to study microbial communities has steadily increased over the last decades. Recently, we have become capable of distinguishing between closely related bacteria, even those belonging to the same species. This has revealed that freshwater bacterial species are actually composed of several subspecies or ecotypes, each with different optimum growth conditions, which replace one another as the environment changes. This intra-species diversity ensures that the species remains present under different environmental conditions, presumably enhancing the stability of the whole ecosystem.
The nature of this intra-species diversity is however unclear. Microbial species are difficult to define, as microorganisms can exchange genetic material via horizontal gene transfer. Because of this, some adaptive genes may not be exclusive of a single bacteria, but instead distributed across a common gene pool. Thus, each ecotype might not actually be a single entity, but a myriad of different bacteria all carrying the adaptive gene while differing otherwise. How are microbial species organized internally? What are the drivers of their diversification? Answering these questions could have large implications in the way we understand microbial species and ecosystems.
The ARAMIS project (Adaptive Radiation in Aquatic MIcrobial Species) aims to advance our understanding on the nature of microbial species, their evolution, and the ecological consequences of intra-species diversity. To achieve this, we collected genomic and metagenomic data from microbial communities in several lakes, and analyzed the internal dynamics of several cosmopolitan freshwater bacterial species through space, time and environmental gradients. We concluded that for some species ecotypes are indeed fuzzy, and that the drivers of intra-species diversification can operate at the gene level rather than the genome level. Furthermore, while this study focused on selection as the driver of intra-species diversification, we found an unexpected signal of dispersal limitation when comparing populations of the same species inhabiting geographically distant lakes.
Within the first year of the project, we generated a database of reference genomes from freshwater species and developed a new bioinformatics algorithm for analyzing intra-species diversity. This algorithm works with the incomplete genomes that are often retrieved from environmental microorganisms, thus ensuring its applicability to all sorts of studies. During the second year, we analyzed the intra-species dynamics of several representative species across hundreds of samples, including time series and spatial transects covering North America, Europe and Asia. We focused on determining how the allelic frequencies and accessory genes changed across time and space in different populations of the same species. Throughout this period, training activities in population genomics and student mentoring were also developed, including the supervision or co-supervision of 1 bachelor students, 4 master students and 1 PhD student.
Our results revealed the existence of certain genomic traits (e.g. presence of accessory genes) associated with adaptation to environmental niches (temperature, or different nitrogen sources). In some cases those traits were not associated to a particular strain within the species yet showed variation across the year, confirming the internal plasticity of microbial species. We also showed the role of homologous recombination (i.e. the ability of genetically close organisms to exchange genetic material) in maintaining species coherence and generating intra-species variability. Recombination rates were however low for some of the species included in our study, suggesting the existence of other processes at play. Our results led us to propose two different models of bacterial microevolution, one based in recurring clonal expansions and another based on steady microevolution. Finally, we found an unexpected influence of geographic distance, with populations of the same species becoming genetically more different as distance increased. This challenges the old assumption that everything is everywhere showing that dispersal limitation is a relevant force in microbial evolution, at least at the short ecoevolutionary timescales involved in intra-species diversification.
These results were communicated in the ISME18 Microbial Ecology Conference (2022) and published in the Microbial Ecology Resources journal. A second publication containing results on biogeography is currently available as a preprint and has been submitted to a high-impact peer reviewed journal.
Our results revealed the existence of certain genomic traits (e.g. presence of accessory genes) associated with adaptation to environmental niches (temperature, or different nitrogen sources). In some cases those traits were not associated to a particular strain within the species yet showed variation across the year, confirming the internal plasticity of microbial species. We also showed the role of homologous recombination (i.e. the ability of genetically close organisms to exchange genetic material) in maintaining species coherence and generating intra-species variability. Recombination rates were however low for some of the species included in our study, suggesting the existence of other processes at play. Our results led us to propose two different models of bacterial microevolution, one based in recurring clonal expansions and another based on steady microevolution. Finally, we found an unexpected influence of geographic distance, with populations of the same species becoming genetically more different as distance increased. This challenges the old assumption that everything is everywhere showing that dispersal limitation is a relevant force in microbial evolution, at least at the short ecoevolutionary timescales involved in intra-species diversification.
These results were communicated in the ISME18 Microbial Ecology Conference (2022) and published in the Microbial Ecology Resources journal. A second publication containing results on biogeography is currently available as a preprint and has been submitted to a high-impact peer reviewed journal.
The progress beyond the state of the art was twofold. First, we developed an open-source tool for tracking bacterial intra-species diversity, which can be adopted by other researchers in order to bring that level of resolution to their own research. Second, we highlighted the previously ignored role of dispersal limitation at the intra-species level in microbial ecosystems, which will surely elicit further research.