Nejvíce citovaný článek - PubMed ID 35659305
Ecogenomics sheds light on diverse lifestyle strategies in freshwater CPR
The SAR11-IIIb genus Fontibacterium within the order 'Ca. Pelagibacterales' is recognized for its ubiquitous presence in freshwater environments. However, cultivation limitations have hampered deeper ecophysiological understanding of this genus, with most data limited to lakes in the Northern Hemisphere. Here we present seven isolates representing two previously undescribed species, along with 93 high-quality metagenome-assembled genomes (MAGs) derived from a global survey across five continents. Phylogenomic analysis revealed 16 species forming nine distinct biogeographic clusters, indicating speciation patterns linked to water temperature and latitude. We observed endemic species restricted to African lakes, and quasi-endemic species confined to the Northern or Southern Hemisphere, which co-exist alongside cosmopolitan species. Metabolic profiling and growth experiments uncovered species- and strain-specific adaptations for nutrient uptake, along with unique pathways for sulfur metabolism. These findings provide a global-scale genomic and ecological overview for this underexplored lineage of freshwater SAR11.
- MeSH
- fylogeneze MeSH
- fylogeografie MeSH
- genom bakteriální MeSH
- jezera mikrobiologie MeSH
- metagenom MeSH
- RNA ribozomální 16S genetika MeSH
- sladká voda * mikrobiologie MeSH
- Publikační typ
- časopisecké články MeSH
- Názvy látek
- RNA ribozomální 16S MeSH
Axenic cultures are essential for studying microbial ecology, evolution, and genomics. Despite the importance of pure cultures, public culture collections are biased towards fast-growing copiotrophs, while many abundant aquatic prokaryotes remain uncultured due to uncharacterized growth requirements and oligotrophic lifestyles. Here, we applied high-throughput dilution-to-extinction cultivation using defined media that mimic natural conditions to samples from 14 Central European lakes, yielding 627 axenic strains. These cultures include 15 genera among the 30 most abundant freshwater bacteria identified via metagenomics, collectively representing up to 72% of genera detected in the original samples (average 40%) and are widespread in freshwater systems globally. Genome-sequenced strains are closely related to metagenome-assembled genomes (MAGs) from the same samples, many of which remain undescribed. We propose a classification of several novel families, genera, and species, including many slowly growing, genome-streamlined oligotrophs that are notoriously underrepresented in public repositories. Our large-scale initiative to cultivate the "uncultivated microbial majority" has yielded a valuable collection of abundant freshwater microbes, characterized by diverse metabolic pathways and lifestyles. This culture collection includes promising candidates for oligotrophic model organisms, suitable for a wide array of ecological studies aimed at advancing our ecological and functional understanding of dominant, yet previously uncultured, taxa.
BACKGROUND: Aerobic anoxygenic phototrophic (AAP) bacteria are heterotrophic bacteria that supply their metabolism with light energy harvested by bacteriochlorophyll-a-containing reaction centers. Despite their substantial contribution to bacterial biomass, microbial food webs, and carbon cycle, their phenology in freshwater lakes remains unknown. Hence, we investigated seasonal variations of AAP abundance and community composition biweekly across 3 years in a temperate, meso-oligotrophic freshwater lake. RESULTS: AAP bacteria displayed a clear seasonal trend with a spring maximum following the bloom of phytoplankton and a secondary maximum in autumn. As the AAP bacteria represent a highly diverse assemblage of species, we followed their seasonal succession using the amplicon sequencing of the pufM marker gene. To enhance the accuracy of the taxonomic assignment, we developed new pufM primers that generate longer amplicons and compiled the currently largest database of pufM genes, comprising 3633 reference sequences spanning all phyla known to contain AAP species. With this novel resource, we demonstrated that the majority of the species appeared during specific phases of the seasonal cycle, with less than 2% of AAP species detected during the whole year. AAP community presented an indigenous freshwater nature characterized by high resilience and heterogenic adaptations to varying conditions of the freshwater environment. CONCLUSIONS: Our findings highlight the substantial contribution of AAP bacteria to the carbon flow and ecological dynamics of lakes and unveil a recurrent and dynamic seasonal succession of the AAP community. By integrating this information with the indicator of primary production (Chlorophyll-a) and existing ecological models, we show that AAP bacteria play a pivotal role in the recycling of dissolved organic matter released during spring phytoplankton bloom. We suggest a potential role of AAP bacteria within the context of the PEG model and their consideration in further ecological models.
- Klíčová slova
- pufM gene, Aerobic anoxygenic phototrophs, Aquatic microbial ecology, Freshwaters, Long-term sampling, Microbial seasonal succession, PEG model, Photoheterotrophs,
- MeSH
- aerobní bakterie genetika metabolismus MeSH
- Bacteria genetika MeSH
- biomasa MeSH
- fototrofní procesy * MeSH
- fytoplankton genetika MeSH
- jezera * mikrobiologie MeSH
- Publikační typ
- časopisecké články MeSH
Telonemia are one of the oldest identified marine protists that for most part of their history have been recognized as a distinct incertae sedis lineage. Today, their evolutionary proximity to the SAR supergroup (Stramenopiles, Alveolates, and Rhizaria) is firmly established. However, their ecological distribution and importance as a natural predatory flagellate, especially in freshwater food webs, still remain unclear. To unravel the distribution and diversity of the phylum Telonemia in freshwater habitats, we examined over a thousand freshwater metagenomes from all over the world. In addition, to directly quantify absolute abundances, we analyzed 407 samples from 97 lakes and reservoirs using Catalyzed Reporter Deposition-Fluorescence in situ Hybridization (CARD-FISH). We recovered Telonemia 18S rRNA gene sequences from hundreds of metagenomic samples from a wide variety of habitats, indicating a global distribution of this phylum. However, even after this extensive sampling, our phylogenetic analysis did not reveal any new major clades, suggesting current molecular surveys are near to capturing the full diversity within this group. We observed excellent concordance between CARD-FISH analyses and estimates of abundances from metagenomes. Both approaches suggest that Telonemia are largely absent from shallow lakes and prefer to inhabit the colder hypolimnion of lakes and reservoirs in the Northern Hemisphere, where they frequently bloom, reaching 10%-20% of the total heterotrophic flagellate population, making them important predatory flagellates in the freshwater food web.
- Klíčová slova
- CARD-FISH, Telonemia, freshwater lakes, metagenomics, microbial food webs, predatory flagellate,
- MeSH
- biodiverzita MeSH
- fylogeneze * MeSH
- hybridizace in situ fluorescenční * MeSH
- jezera mikrobiologie parazitologie MeSH
- metagenom MeSH
- metagenomika MeSH
- RNA ribozomální 18S * genetika MeSH
- sladká voda * mikrobiologie parazitologie MeSH
- Publikační typ
- časopisecké články MeSH
- Názvy látek
- RNA ribozomální 18S * MeSH
The evolutionary trajectory of Methylophilaceae includes habitat transitions from freshwater sediments to freshwater and marine pelagial that resulted in genome reduction (genome-streamlining) of the pelagic taxa. However, the extent of genetic similarities in the genomic structure and microdiversity of the two genome-streamlined pelagic lineages (freshwater "Ca. Methylopumilus" and the marine OM43 lineage) has so far never been compared. Here, we analyzed complete genomes of 91 "Ca. Methylopumilus" strains isolated from 14 lakes in Central Europe and 12 coastal marine OM43 strains. The two lineages showed a remarkable niche differentiation with clear species-specific differences in habitat preference and seasonal distribution. On the other hand, we observed a synteny preservation in their genomes by having similar locations and types of flexible genomic islands (fGIs). Three main fGIs were identified: a replacement fGI acting as phage defense, an additive fGI harboring metabolic and resistance-related functions, and a tycheposon containing nitrogen-, thiamine-, and heme-related functions. The fGIs differed in relative abundances in metagenomic datasets suggesting different levels of variability ranging from strain-specific to population-level adaptations. Moreover, variations in one gene seemed to be responsible for different growth at low substrate concentrations and a potential biogeographic separation within one species. Our study provides a first insight into genomic microdiversity of closely related taxa within the family Methylophilaceae and revealed remarkably similar dynamics involving mobile genetic elements and recombination between freshwater and marine family members.
- Klíčová slova
- Methylophilaceae, cultivation, genome-streamlined bacteria, genomic islands, genomic microdiversity, genomics,
- MeSH
- fylogeneze MeSH
- genom bakteriální MeSH
- genomové ostrovy MeSH
- jezera MeSH
- Methylophilaceae * MeSH
- Publikační typ
- časopisecké články MeSH
Acidobacteriota are abundant in soil, peatlands, and sediments, but their ecology in freshwater environments remains understudied. UBA12189, an Acidobacteriota genus, is an uncultivated, genome-streamlined lineage with a small genome size found in aquatic environments where detailed genomic analyses are lacking. Here, we analyzed 66 MAGs of UBA12189 (including one complete genome) from freshwater lakes and rivers in Europe, North America, and Asia. UBA12189 has small genome sizes (<1.4 Mbp), low GC content, and a highly diverse pangenome. In freshwater lakes, this bacterial lineage is abundant from the surface waters (epilimnion) down to a 300-m depth (hypolimnion). UBA12189 appears to be free-living from CARD-FISH analysis. When compared to other genome-streamlined bacteria such as Nanopelagicales and Methylopumilus, genome reduction has caused UBA12189 to have a more limited metabolic repertoire in carbon, sulfur, and nitrogen metabolisms, limited numbers of membrane transporters, as well as a higher degree of auxotrophy for various amino acids, vitamins, and reduced sulfur. Despite having reduced genomes, UBA12189 encodes proteorhodopsin, complete biosynthesis pathways for heme and vitamin K2, cbb3-type cytochrome c oxidases, and heme-requiring enzymes. These genes may give a selective advantage during the genome streamlining process. We propose the new genus Acidiparvus, with two new species named "A. lacustris" and "A. fluvialis". Acidiparvus is the first described genome-streamlined lineage under the phylum Acidobacteriota, which is a free-living, slow-growing scavenger in freshwater environments.
- Klíčová slova
- Acidiparvus, aquatic microbial ecology, freshwater lakes, genome streamlined Acidobacteriota metagenomics, genome streamlined bacteria,
- Publikační typ
- časopisecké články MeSH
In freshwater systems, cyanobacteria are strong competitors under enhanced temperature and eutrophic conditions. Understanding their adaptive and evolutionary potential to multiple environmental states allows us to accurately predict their response to future conditions. To better understand if the combined impacts of temperature and nutrient limitation could suppress the cyanobacterial blooms, a single strain of Microcystis aeruginosa was inoculated into natural phytoplankton communities with different nutrient conditions: oligotrophic, eutrophic and eutrophic with the addition of bentophos. We found that the use of the bentophos treatment causes significant differences in prokaryotic and eukaryotic communities. This resulted in reduced biodiversity among the eukaryotes and a decline in cyanobacterial abundance suggesting phosphorus limitation had a strong impact on the community structure. The low temperature during the experiment lead to the disappearance of M. aeruginosa in all treatments and gave other phytoplankton groups a competitive advantage leading to the dominance of the eukaryotic families that have diverse morphologies and nutritional modes. These results show cyanobacteria have a reduced competitive advantage under certain temperature and nutrient limiting conditions and therefore, controlling phosphorus concentrations could be a possible mitigation strategy for managing harmful cyanobacterial blooms in a future warmer climate.
- MeSH
- eutrofizace MeSH
- fosfor MeSH
- fytoplankton MeSH
- jezera chemie MeSH
- lidé MeSH
- Microcystis * MeSH
- sinice * MeSH
- teplota MeSH
- Check Tag
- lidé MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- fosfor MeSH
