Nejvíce citovaný článek - PubMed ID 25942006
The ecology of pelagic freshwater methylotrophs assessed by a high-resolution monitoring and isolation campaign
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.
- Publikační typ
- časopisecké články 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
BACKGROUND: Planktonic microbial communities have critical impacts on the pelagic food web and water quality status in freshwater ecosystems, yet no general model of bacterial community assembly linked to higher trophic levels and hydrodynamics has been assessed. In this study, we utilized a 2-year survey of planktonic communities from bacteria to zooplankton in three freshwater reservoirs to investigate their spatiotemporal dynamics. RESULTS: We observed site-specific occurrence and microdiversification of bacteria in lacustrine and riverine environments, as well as in deep hypolimnia. Moreover, we determined recurrent bacterial seasonal patterns driven by both biotic and abiotic conditions, which could be integrated into the well-known Plankton Ecology Group (PEG) model describing primarily the seasonalities of larger plankton groups. Importantly, bacteria with different ecological potentials showed finely coordinated successions affiliated with four seasonal phases, including the spring bloom dominated by fast-growing opportunists, the clear-water phase associated with oligotrophic ultramicrobacteria, the summer phase characterized by phytoplankton bloom-associated bacteria, and the fall/winter phase driven by decay-specialists. CONCLUSIONS: Our findings elucidate the major principles driving the spatiotemporal microbial community distribution in freshwater ecosystems. We suggest an extension to the original PEG model by integrating new findings on recurrent bacterial seasonal trends. Video Abstract.
- Klíčová slova
- Freshwater reservoirs, Microbial communities, Microdiversity, PEG model, Spatiotemporal dynamics,
- MeSH
- Bacteria genetika MeSH
- ekosystém * MeSH
- fytoplankton MeSH
- plankton * MeSH
- roční období MeSH
- zooplankton MeSH
- zvířata MeSH
- Check Tag
- zvířata MeSH
- Publikační typ
- audiovizuální média MeSH
- časopisecké články MeSH
- práce podpořená grantem MeSH
BACKGROUND: The phytoplankton spring bloom in freshwater habitats is a complex, recurring, and dynamic ecological spectacle that unfolds at multiple biological scales. Although enormous taxonomic shifts in microbial assemblages during and after the bloom have been reported, genomic information on the microbial community of the spring bloom remains scarce. RESULTS: We performed a high-resolution spatio-temporal sampling of the spring bloom in a freshwater reservoir and describe a multitude of previously unknown taxa using metagenome-assembled genomes of eukaryotes, prokaryotes, and viruses in combination with a broad array of methodologies. The recovered genomes reveal multiple distributional dynamics for several bacterial groups with progressively increasing stratification. Analyses of abundances of metagenome-assembled genomes in concert with CARD-FISH revealed remarkably similar in situ doubling time estimates for dominant genome-streamlined microbial lineages. Discordance between quantitations of cryptophytes arising from sequence data and microscopic identification suggested the presence of hidden, yet extremely abundant aplastidic cryptophytes that were confirmed by CARD-FISH analyses. Aplastidic cryptophytes are prevalent throughout the water column but have never been considered in prior models of plankton dynamics. We also recovered the first metagenomic-assembled genomes of freshwater protists (a diatom and a haptophyte) along with thousands of giant viral genomic contigs, some of which appeared similar to viruses infecting haptophytes but owing to lack of known representatives, most remained without any indication of their hosts. The contrasting distribution of giant viruses that are present in the entire water column to that of parasitic perkinsids residing largely in deeper waters allows us to propose giant viruses as the biological agents of top-down control and bloom collapse, likely in combination with bottom-up factors like a nutrient limitation. CONCLUSION: We reconstructed thousands of genomes of microbes and viruses from a freshwater spring bloom and show that such large-scale genome recovery allows tracking of planktonic succession in great detail. However, integration of metagenomic information with other methodologies (e.g., microscopy, CARD-FISH) remains critical to reveal diverse phenomena (e.g., distributional patterns, in situ doubling times) and novel participants (e.g., aplastidic cryptophytes) and to further refine existing ecological models (e.g., factors affecting bloom collapse). This work provides a genomic foundation for future approaches towards a fine-scale characterization of the organisms in relation to the rapidly changing environment during the course of the freshwater spring bloom. Video Abstract.
- MeSH
- Bacteria MeSH
- Eukaryota genetika MeSH
- metagenom * MeSH
- plankton MeSH
- sladká voda MeSH
- viry * genetika MeSH
- voda MeSH
- Publikační typ
- audiovizuální média MeSH
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- voda MeSH
Small lakes and ponds occupy an enormous surface area of inland freshwater and represent an important terrestrial-water interface. Disturbances caused by extreme weather events can have substantial effects on these ecosystems. Here, we analysed the dynamics of nutrients and the entire plankton community in two flood events and afterwards, when quasi-stable conditions were established, to investigate the effect of such disturbances on a small forest pond. We show that floodings result in repeated washout of resident organisms and hundredfold increases in nutrient load. Despite this, the microbial community recovers to a predisturbance state within two weeks of flooding through four well-defined succession phases. Reassembly of phytoplankton and especially zooplankton takes up to two times longer and features repetitive and adaptive patterns. Release of dissolved nutrients from the pond is associated with inflow rates and community recovery, and returns to predisturbance levels before microbial compositions recover. Our findings shed light on the mechanisms underlying functional resilience of small waterbodies and are relevant to global change-induced increases in weather extremes.
- MeSH
- déšť * MeSH
- extrémní počasí * MeSH
- lesy MeSH
- mikrobiota * MeSH
- plankton růst a vývoj MeSH
- potravní řetězec MeSH
- řeky chemie mikrobiologie MeSH
- rybníky chemie mikrobiologie MeSH
- sladká voda chemie mikrobiologie MeSH
- záplavy MeSH
- živiny analýza MeSH
- zvířata MeSH
- Check Tag
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
The most abundant aquatic microbes are small in cell and genome size. Genome-streamlining theory predicts gene loss caused by evolutionary selection driven by environmental factors, favouring superior competitors for limiting resources. However, evolutionary histories of such abundant, genome-streamlined microbes remain largely unknown. Here we reconstruct the series of steps in the evolution of some of the most abundant genome-streamlined microbes in freshwaters ("Ca. Methylopumilus") and oceans (marine lineage OM43). A broad genomic spectrum is visible in the family Methylophilaceae (Betaproteobacteria), from sediment microbes with medium-sized genomes (2-3 Mbp genome size), an occasionally blooming pelagic intermediate (1.7 Mbp), and the most reduced pelagic forms (1.3 Mbp). We show that a habitat transition from freshwater sediment to the relatively oligotrophic pelagial was accompanied by progressive gene loss and adaptive gains. Gene loss has mainly affected functions not necessarily required or advantageous in the pelagial or is encoded by redundant pathways. Likewise, we identified genes providing adaptations to oligotrophic conditions that have been transmitted horizontally from pelagic freshwater microbes. Remarkably, the secondary transition from the pelagial of lakes to the oceans required only slight modifications, i.e., adaptations to higher salinity, gained via horizontal gene transfer from indigenous microbes. Our study provides first genomic evidence of genome reduction taking place during habitat transitions. In this regard, the family Methylophilaceae is an exceptional model for tracing the evolutionary history of genome streamlining as such a collection of evolutionarily related microbes from different habitats is rare in the microbial world.
- MeSH
- délka genomu MeSH
- ekosystém * MeSH
- fylogeneze MeSH
- fyziologická adaptace MeSH
- genom bakteriální * MeSH
- geologické sedimenty mikrobiologie MeSH
- jezera mikrobiologie MeSH
- Methylophilaceae klasifikace genetika izolace a purifikace fyziologie MeSH
- molekulární evoluce MeSH
- mořská voda mikrobiologie MeSH
- přenos genů horizontální MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
Freshwater environments teem with microbes that do not have counterparts in culture collections or genetic data available in genomic repositories. Currently, our apprehension of evolutionary ecology of freshwater bacteria is hampered by the difficulty to establish organism models for the most representative clades. To circumvent the bottlenecks inherent to the cultivation-based techniques, we applied ecogenomics approaches in order to unravel the evolutionary history and the processes that drive genome architecture in hallmark freshwater lineages from the phylum Planctomycetes. The evolutionary history inferences showed that sediment/soil Planctomycetes transitioned to aquatic environments, where they gave rise to new freshwater-specific clades. The most abundant lineage was found to have the most specialised lifestyle (increased regulatory genetic circuits, metabolism tuned for mineralization of proteinaceous sinking aggregates, psychrotrophic behaviour) within the analysed clades and to harbour the smallest freshwater Planctomycetes genomes, highlighting a genomic architecture shaped by niche-directed evolution (through loss of functions and pathways not needed in the newly acquired freshwater niche).
BACKGROUND: Representatives of the phylum Chloroflexi, though reportedly highly abundant in the extensive deep water habitats of both marine (SAR202 up to 30% of total prokaryotes) and freshwater (CL500-11 up to 26% of total prokaryotes), remain uncultivated and uncharacterized. There are few metagenomic studies on marine Chloroflexi representatives, while the pelagic freshwater Chloroflexi community is largely unknown except for a single metagenome-assembled genome of CL500-11. RESULTS: Here, we provide the first extensive examination of the community composition of this cosmopolitan phylum in a range of pelagic habitats (176 datasets) and highlight the impact of salinity and depth on their phylogenomic composition. Reconstructed genomes (53 in total) provide a perspective on the phylogeny, metabolism, and distribution of three novel classes and two family-level taxa within the phylum Chloroflexi. We unraveled a remarkable genomic diversity of pelagic freshwater Chloroflexi representatives that thrive not only in the hypolimnion as previously suspected, but also in the epilimnion. Our results suggest that the lake hypolimnion provides a globally stable habitat reflected in lower species diversity among hypolimnion-specific CL500-11 and TK10 clusters in distantly related lakes compared to a higher species diversity of the epilimnion-specific SL56 cluster. Cell volume analyses show that the CL500-11 are among the largest prokaryotic cells in the water column of deep lakes and with a biomass to abundance ratio of two they significantly contribute to the deep lake carbon flow. Metabolic insights indicate participation of JG30-KF-CM66 representatives in the global cobalamin production via cobinamide to cobalamin salvage pathway. CONCLUSIONS: Extending phylogenomic comparisons to brackish and marine habitats suggests salinity as the major influencer of the community composition of the deep-dwelling Chloroflexi in marine (SAR202) and freshwater (CL500-11) habitats as both counterparts thrive in intermediate brackish salinity; however, freshwater habitats harbor the most phylogenetically diverse community of pelagic Chloroflexi representatives that reside both in epi- and hypolimnion.
- Klíčová slova
- CARD-FISH, Chloroflexi, Freshwater ecology, Metagenomics,
- MeSH
- Chloroflexi klasifikace genetika izolace a purifikace MeSH
- DNA bakterií genetika MeSH
- ekosystém MeSH
- fylogeneze MeSH
- genom bakteriální genetika MeSH
- jezera mikrobiologie MeSH
- metagenom genetika MeSH
- plankton klasifikace genetika MeSH
- RNA ribozomální 16S genetika MeSH
- salinita MeSH
- sekvenční analýza DNA MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Geografické názvy
- Česká republika MeSH
- Názvy látek
- DNA bakterií MeSH
- RNA ribozomální 16S MeSH
Freshwater systems are characterized by an enormous diversity of eukaryotic protists and prokaryotic taxa. The community structures in different lakes are thereby influenced by factors such as habitat size, lake chemistry, biotic interactions, and seasonality. In our study, we used high throughput 454 sequencing to study the diversity and temporal changes of prokaryotic and eukaryotic planktonic communities in three Austrian lakes during the ice-free season. In the following year, one lake was sampled again with a reduced set of sampling dates to observe reoccurring patterns. Cluster analyses (based on SSU V9 (eukaryotic) and V4 (prokaryotic) OTU composition) grouped samples according to their origin followed by separation into seasonal clusters, indicating that each lake has a unique signature based on OTU composition. These results suggest a strong habitat-specificity of microbial communities and in particular of community patterns at the OTU level. A comparison of the prokaryotic and eukaryotic datasets via co-inertia analysis (CIA) showed a consistent clustering of prokaryotic and eukaryotic samples, probably reacting to the same environmental forces (e.g., pH, conductivity). In addition, the shifts in eukaryotic and bacterioplanktonic communities generally occurred at the same time and on the same scale. Regression analyses revealed a linear relationship between an increase in Bray-Curtis dissimilarities and elapsed time. Our study shows a pronounced coupling between bacteria and eukaryotes in seasonal samplings of the three analyzed lakes. However, our temporal resolution (biweekly sampling) and data on abiotic factors were insufficient to determine if this was caused by direct biotic interactions or by reacting to the same seasonally changing environmental forces.
- Klíčová slova
- Seasonality, diversity, eukaryotic plankton, freshwater, prokaryotic plankton, protist,
- Publikační typ
- časopisecké články MeSH