Ecogenomics of genome-streamlined freshwater methylotrophs
Project leader: Michaela Salcher
The most abundant planktonic microbes have reduced genomes and streamlining theory predicts that gene loss is caused by evolutionary selection driven by environmental factors. Yet the evolutionary path of streamlining remains unknown because of obstacles in establishing axenic cultures of such microbes. We developed a targeted isolation technique for abundant genome-streamlined freshwater methylotrophs: ‘Ca. Methylopumilus planktonicus’ (Betaproteobacteria, 1.3 Mbp genome size), that are ideal model organisms for studying microdiversification patterns and the evolution of genome-streamlining per se. The closest relatives of ‘Ca. M. planktonicus’ inhabit lake sediments and the pelagial of oceans, and we propose that the evolutionary origin of the family can be traced back to sediment microbes with medium-sized genomes. Whole genome sequencing of 150 strains and deep sequencing of metagenomes will allow comparative population genomics with the aim to disentangle the underlying ecological reasons for the widespread but yet enigmatic phenomenon of genomestreamlining in aquatic microbes.
The aim of the project is using targeted isolation and whole-genome-sequencing of oligotrophic freshwater ‘Ca. Methylopumilus planktonicus’ (Betaproteobacteria) together with metagenomics to study the evolution of genome-streamlining in planktonic microbes. Identifying microdiversification patterns in closely related taxa.
Financial support: Czech Science Foundation; Project No.: 19-23469S, duration: 2019 - 2021
Main publications related to the project:
Chiriac M., Haber M., Salcher M.M. (2023) Adaptive genetic traits in pelagic freshwater microbes. Environmental Microbiology 25: 606–641. DOI: 10.1111/1462-2920.16313
Layoun P., López-Pérez M., Haro-Moreno J.M., Haber M., Thrash J.C., Henson M.W., Kavagutti V., Ghai R., Salcher M.M.(2024) Flexible genomic island conservation across freshwater and marine Methylophilaceae. The ISME Journal 18: wrad036. DOI: 10.1093/ismejo/wrad036
Salcher M.M., Schaefle D., Kaspar M., Neuenschwander S., Ghai R. (2019) Evolution in action: habitat transition from sediment to the pelagial leads to genome streamlining in Methylophilaceae. The ISME Journal 13: 2764–2777. DOI: 10.1038/s41396-019-0471-3
Other publications related to the project or used data generated in this project:
Chiriac M., Bulzu P., Andrei A.S., Okazaki Y., Nakano S., Haber M., Kavagutti V., Layoun P., Ghai R., Salcher M.M. (2022) Ecogenomics sheds light on diverse lifestyle strategies in freshwater CPR. Microbiome 10: 84. DOI: 10.1186/s40168-022-01274-3
Kavagutti V., Bulzu P., Chiriac M., Salcher M.M., Mukherjee I., Shabarova T.,, Grujčić V., Mehrshad M., Kasalický V., Andrei A.S., Jezberová J., Seďa J., Rychtecký P., Znachor P., Šimek K., Ghai R. (2023) High‑resolution metagenomic reconstruction of the freshwater spring bloom. Microbiome 11: 15. DOI: 10.1186/s40168-022-01451-4
Mujakic I., Andrei A., Shabarova T., Kolesár Fecskeová L., Salcher M.M., Piwosz K., Ghai R., Koblížek M. (2021) Common presence of phototrophic Gemmatimonadota in temperate freshwater lakes. mSystems 6: e01241-20. DOI: 10.1128/mSystems.01241-20
Mukherjee I., Salcher M.M., Andrei A., Kavagutti V., Shabarova T., Grujčić V., Haber M., Layoun P., Hodoki Y., Nakano S., Šimek K., Ghai R. (2020) A freshwater radiation of diplonemids. Environmental Microbiology 22: 4658–4668. DOI: doi.org/10.1101/2020.05.14.095992
Ngugi D.K., Salcher M.M., Andrei A.S., Ghai R., Klotz F., Chiriac M., Ionescu D., Büsing P., Grossart H., Xing P., Priscu J.C., Alymkulov S., Pester M. (2023) Postglacial adaptations enabled colonization and quasi-clonal dispersal of ammonia-oxidizing archaea in modern European large lakes. Sciences Advances 9: eadc9392. DOI: 10.1126/sciadv.adc9392
Okazaki Y., Fujinaga S., Salcher M.M., Callieri C., Tanaka A., Kohzu A., Oyagi H., Tamaki H., Nakano S. (2021) Microdiversity and phylogeographic diversification of bacterioplankton in pelagic freshwater systems revealed through long-read amplicon sequencing. Microbiome 9: 24. DOI: 10.1186/s40168-020-00974-y
Park H., Shabarova T., Salcher M.M., Kosová L., Rychtecký P., Mukherjee I., Šimek K., Porcal P., Seďa J., Znachor P., Kasalický V. (2023) In the right place, at the right time: the integration of bacteria into the Plankton Ecology Group model. Microbiome 11: 112. DOI: 10.1186/s40168-023-01522-0
Piwosz K., Shabarova T., Pernthaler J., Posch T., Šimek K., Porcal P., Salcher M.M. (2020) Bacterial and eukaryotic small-subunit amplicon data do not provide a quantitative picture of microbial communities, but they are reliable in the context of ecological interpretations. mSphere 5: e00052-20. DOI: 10.1128/mSphere.00052-20
Shabarova T., Salcher M.M., Porcal P., Znachor P., Nedoma J., Grossart H., Seďa J., Hejzlar J., Šimek K. (2021) Recovery of freshwater microbial communities after extreme rain events is mediated by cyclic succession. Nature Microbiology 6: 479–488. DOI: 10.1038/s41564-020-00852-1
Wong H., Bulzu P.-A., Ghai R., Chiriac M.-C., Salcher M.M. (2024) Ubiquitous genome streamlined Acidobacteriota in freshwater environments. ISME Communications 4: ycae124. DOI: 10.1093/ismeco/ycae124
