Nejvíce citovaný článek - PubMed ID 28810712
Genomic Analysis of the Evolution of Phototrophy among Haloalkaliphilic Rhodobacterales
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
During their long evolution, anoxygenic phototrophic bacteria have inhabited a wide variety of natural habitats and developed specific strategies to cope with the challenges of any particular environment. Expression, assembly, and safe operation of the photosynthetic apparatus must be regulated to prevent reactive oxygen species generation under illumination in the presence of oxygen. Here, we report on the photoheterotrophic Sediminicoccus sp. strain KRV36, which was isolated from a cold stream in north-western Iceland, 30 km south of the Arctic Circle. In contrast to most aerobic anoxygenic phototrophs, which stop pigment synthesis when illuminated, strain KRV36 maintained its bacteriochlorophyll synthesis even under continuous light. Its cells also contained between 100 and 180 chromatophores, each accommodating photosynthetic complexes that exhibit an unusually large carotenoid absorption spectrum. The expression of photosynthesis genes in dark-adapted cells was transiently downregulated in the first 2 hours exposed to light but recovered to the initial level within 24 hours. An excess of membrane-bound carotenoids as well as high, constitutive expression of oxidative stress response genes provided the required potential for scavenging reactive oxygen species, safeguarding bacteriochlorophyll synthesis and photosystem assembly. The unique cellular architecture and an unusual gene expression pattern represent a specific adaptation that allows the maintenance of anoxygenic phototrophy under arctic conditions characterized by long summer days with relatively low irradiance.IMPORTANCEThe photoheterotrophic bacterium Sediminicoccus sp. KRV36 was isolated from a cold stream in Iceland. It expresses its photosynthesis genes, synthesizes bacteriochlorophyll, and assembles functional photosynthetic complexes under continuous light in the presence of oxygen. Unraveling the molecular basis of this ability, which is exceptional among aerobic anoxygenic phototrophic species, will help to understand the evolution of bacterial photosynthesis in response to changing environmental conditions. It might also open new possibilities for genetic engineering of biotechnologically relevant phototrophs, with the aim of increasing photosynthetic activity and their tolerance to reactive oxygen species.
- Klíčová slova
- AAP, Proteobacteria, Sediminicoccus, gene expression, light adaptation, photosynthesis,
- MeSH
- Bacteria metabolismus MeSH
- bakteriochlorofyly * metabolismus MeSH
- fotosyntetická reakční centra (proteinové komplexy) * genetika MeSH
- fotosyntéza genetika MeSH
- kyslík metabolismus MeSH
- reaktivní formy kyslíku MeSH
- Publikační typ
- časopisecké články MeSH
- Geografické názvy
- Island MeSH
- Názvy látek
- bakteriochlorofyly * MeSH
- fotosyntetická reakční centra (proteinové komplexy) * MeSH
- kyslík MeSH
- reaktivní formy kyslíku MeSH
Aerobic anoxygenic photoheterotrophic (AAP) bacteria represent a functional group of prokaryotic organisms that harvests light energy using bacteriochlorophyll-containing photosynthetic reaction centers. They represent an active and rapidly growing component of freshwater bacterioplankton, with the highest numbers observed usually in summer. Species diversity of freshwater AAP bacteria has been studied before in lakes, but its seasonal dynamics remain unknown. In this report, we analysed temporal changes in the composition of the phototrophic community in an oligo-mesotrophic freshwater lake using amplicon sequencing of the pufM marker gene. The AAP community was dominated by phototrophic Gammaproteobacteria and Alphaproteobacteria, with smaller contribution of phototrophic Chloroflexota and Gemmatimonadota. Phototrophic Eremiobacteriota or members of Myxococcota were not detected. Interestingly, some AAP taxa, such as Limnohabitans, Rhodoferax, Rhodobacterales or Rhizobiales, were permanently present over the sampling period, while others, such as Sphingomonadales, Rhodospirillales or Caulobacterales appeared only transiently. The environmental factors that best explain the seasonal changes in AAP community were temperature, concentrations of oxygen and dissolved organic matter.
Photoheterotrophic bacteria represent an important part of aquatic microbial communities. There exist two fundamentally different light-harvesting systems: bacteriochlorophyll-containing reaction centers or rhodopsins. Here, we report a photoheterotrophic Sphingomonas strain isolated from an oligotrophic lake, which contains complete sets of genes for both rhodopsin-based and bacteriochlorophyll-based phototrophy. Interestingly, the identified genes were not expressed when cultured in liquid organic media. Using reverse transcription quantitative PCR (RT-qPCR), RNA sequencing, and bacteriochlorophyll a quantification, we document that bacteriochlorophyll synthesis was repressed by high concentrations of glucose or galactose in the medium. Coactivation of photosynthesis genes together with genes for TonB-dependent transporters suggests the utilization of light energy for nutrient import. The photosynthetic units were formed by ring-shaped light-harvesting complex 1 and reaction centers with bacteriochlorophyll a and spirilloxanthin as the main light-harvesting pigments. The identified rhodopsin gene belonged to the xanthorhodopsin family, but it lacks salinixanthin antenna. In contrast to bacteriochlorophyll, the expression of xanthorhodopsin remained minimal under all experimental conditions tested. Since the gene was found in the same operon as a histidine kinase, we propose that it might serve as a light sensor. Our results document that photoheterotrophic Sphingomonas bacteria use the energy of light under carbon-limited conditions, while under carbon-replete conditions, they cover all their metabolic needs through oxidative phosphorylation.IMPORTANCE Phototrophic organisms are key components of many natural environments. There exist two main phototrophic groups: species that collect light energy using various kinds of (bacterio)chlorophylls and species that utilize rhodopsins. Here, we present a freshwater bacterium Sphingomonas sp. strain AAP5 which contains genes for both light-harvesting systems. We show that bacteriochlorophyll-based reaction centers are repressed by light and/or glucose. On the other hand, the rhodopsin gene was not expressed significantly under any of the experimental conditions. This may indicate that rhodopsin in Sphingomonas may have other functions not linked to bioenergetics.
- Klíčová slova
- Sphingomonadaceae, aerobic anoxygenic phototrophic bacteria, bacteriochlorophyll a, gene expression, photosynthesis gene cluster, rhodopsin,
- Publikační typ
- časopisecké články MeSH
All purple photosynthetic bacteria contain RC-LH1 'Core' complexes. The structure of this complex from Rhodobacter sphaeroides, Rhodopseudomonas palustris and Thermochromatium tepidum has been solved using X-ray crystallography. Recently, the application of single particle cryo-EM has revolutionised structural biology and the structure of the RC-LH1 'Core' complex from Blastochloris viridis has been solved using this technique, as well as the complex from the non-purple Chloroflexi species, Roseiflexus castenholzii. It is apparent that these structures are variations on a theme, although with a greater degree of structural diversity within them than previously thought. Furthermore, it has recently been discovered that the only phototrophic representative from the phylum Gemmatimonadetes, Gemmatimonas phototrophica, also contains a RC-LH1 'Core' complex. At present only a low-resolution EM-projection map exists but this shows that the Gemmatimonas phototrophica complex contains a double LH1 ring. This short review compares these different structures and looks at the functional significance of these variations from two main standpoints: energy transfer and quinone exchange.
- Klíčová slova
- Anoxygenic phototrophs, Light harvesting, Purple photosynthetic bacteria, RC–LH1, Reaction centres, Structures,
- MeSH
- bakteriální proteiny chemie genetika metabolismus MeSH
- benzochinony metabolismus MeSH
- Chromatiaceae genetika metabolismus MeSH
- fotosyntetická reakční centra (proteinové komplexy) chemie genetika metabolismus MeSH
- fotosyntéza * MeSH
- genetická variace MeSH
- konformace proteinů MeSH
- molekulární modely MeSH
- přenos energie MeSH
- Rhodobacter sphaeroides genetika metabolismus MeSH
- Rhodopseudomonas genetika metabolismus MeSH
- světlosběrné proteinové komplexy chemie genetika metabolismus MeSH
- vztahy mezi strukturou a aktivitou MeSH
- Publikační typ
- časopisecké články MeSH
- přehledy MeSH
- srovnávací studie MeSH
- Názvy látek
- bakteriální proteiny MeSH
- benzochinony MeSH
- fotosyntetická reakční centra (proteinové komplexy) MeSH
- quinone MeSH Prohlížeč
- světlosběrné proteinové komplexy MeSH
BACKGROUND: The planetary sulfur cycle is a complex web of chemical reactions that can be microbial-mediated or can occur spontaneously in the environment, depending on the temperature and pH. Inorganic sulfur compounds can serve as energy sources for specialized prokaryotes and are important substrates for microbial growth in general. Here, we investigate dissimilatory sulfur cycling in the brine and sediments of a southwestern Siberian soda lake characterized by an extremely high pH and salinity, combining meta-omics analyses of its uniquely adapted highly diverse prokaryote communities with biogeochemical profiling to identify key microbial players and expand our understanding of sulfur cycling under haloalkaline conditions. RESULTS: Peak microbial activity was found in the top 4 cm of the sediments, a layer with a steep drop in oxygen concentration and redox potential. The majority of sulfur was present as sulfate or iron sulfide. Thiosulfate was readily oxidized by microbes in the presence of oxygen, but oxidation was partially inhibited by light. We obtained 1032 metagenome-assembled genomes, including novel population genomes of characterized colorless sulfur-oxidizing bacteria (SOB), anoxygenic purple sulfur bacteria, heterotrophic SOB, and highly active lithoautotrophic sulfate reducers. Surprisingly, we discovered the potential for nitrogen fixation in a new genus of colorless SOB, carbon fixation in a new species of phototrophic Gemmatimonadetes, and elemental sulfur/sulfite reduction in the "Candidatus Woesearchaeota." Polysulfide/thiosulfate and tetrathionate reductases were actively transcribed by various (facultative) anaerobes. CONCLUSIONS: The recovery of over 200 genomes that encoded enzymes capable of catalyzing key reactions in the inorganic sulfur cycle indicates complete cycling between sulfate and sulfide at moderately hypersaline and extreme alkaline conditions. Our results suggest that more taxonomic groups are involved in sulfur dissimilation than previously assumed.
- Klíčová slova
- Gemmatimonadetes, Haloalkaliphiles, Metagenomics, Metatranscriptomics, Nitrogen fixation, Polysulfide, Soda lake, Tetrathionate, Thiosulfate, Woesearchaeota,
- MeSH
- Archaea klasifikace genetika metabolismus MeSH
- Bacteria klasifikace genetika metabolismus MeSH
- fylogeneze MeSH
- jezera chemie mikrobiologie MeSH
- koncentrace vodíkových iontů MeSH
- metagenom MeSH
- oxidace-redukce MeSH
- salinita MeSH
- síra analýza metabolismus MeSH
- soli chemie MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Geografické názvy
- Sibiř MeSH
- Názvy látek
- brine MeSH Prohlížeč
- síra MeSH
- soli MeSH
In Bacteria, chromosome replication starts at a single origin of replication and proceeds on both replichores. Due to its asymmetric nature, replication influences chromosome structure and gene organization, mutation rate, and expression. To date, little is known about the distribution of highly conserved genes over the bacterial chromosome. Here, we used a set of 101 fully sequenced Rhodobacteraceae representatives to analyze the relationship between conservation of genes within this family and their distance from the origin of replication. Twenty-two of the analyzed species had core genes clustered significantly closer to the origin of replication with representatives of the genus Celeribacter being the most apparent example. Interestingly, there were also eight species with the opposite organization. In particular, Rhodobaca barguzinensis and Loktanella vestfoldensis showed a significant increase of core genes with distance from the origin of replication. The uneven distribution of low-conserved regions is in particular pronounced for genomes in which the halves of one replichore differ in their conserved gene content. Phage integration and horizontal gene transfer partially explain the scattered nature of Rhodobacteraceae genomes. Our findings lay the foundation for a better understanding of bacterial genome evolution and the role of replication therein.
- Klíčová slova
- Rhodobacteraceae, genome architecture, genome evolution, origin of replication,
- MeSH
- bakteriální chromozomy genetika MeSH
- bakteriální proteiny genetika MeSH
- fylogeneze * MeSH
- genom bakteriální * MeSH
- regulace genové exprese u bakterií MeSH
- replikace DNA MeSH
- Rhodobacteraceae genetika MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- bakteriální proteiny MeSH
Soda lakes, with their high salinity and high pH, pose a very challenging environment for life. Microorganisms living in these harsh conditions have had to adapt their physiology and gene inventory. Therefore, we analyzed the complete genome of the haloalkaliphilic photoheterotrophic bacterium Rhodobaca barguzinensis strain alga05. It consists of a 3,899,419 bp circular chromosome with 3624 predicted coding sequences. In contrast to most of Rhodobacterales, this strain lacks any extrachromosomal elements. To identify the genes responsible for adaptation to high pH, we compared the gene inventory in the alga05 genome with genomes of 17 reference strains belonging to order Rhodobacterales. We found that all haloalkaliphilic strains contain the mrpB gene coding for the B subunit of the MRP Na+/H+ antiporter, while this gene is absent in all non-alkaliphilic strains, which indicates its importance for adaptation to high pH. Further analysis showed that alga05 requires organic carbon sources for growth, but it also contains genes encoding the ethylmalonyl-CoA pathway for CO2 fixation. Remarkable is the genetic potential to utilize organophosphorus compounds as a source of phosphorus. In summary, its genetic inventory indicates a large flexibility of the alga05 metabolism, which is advantageous in rapidly changing environmental conditions in soda lakes.
- Klíčová slova
- Element cycles, Genome annotation, Haloalkaliphiles, Rhodobacterales, Soda lake,
- MeSH
- anotace sekvence MeSH
- fyziologická adaptace MeSH
- genom bakteriální * MeSH
- jezera mikrobiologie MeSH
- Rhodobacteraceae genetika fyziologie MeSH
- Publikační typ
- časopisecké články MeSH
The capacity for anoxygenic photosynthesis is scattered throughout the phylogeny of the Proteobacteria. Their photosynthesis genes are typically located in a so-called photosynthesis gene cluster (PGC). It is unclear (i) whether phototrophy is an ancestral trait that was frequently lost or (ii) whether it was acquired later by horizontal gene transfer. We investigated the evolution of phototrophy in 105 genome-sequenced Rhodobacteraceae and provide the first unequivocal evidence for the horizontal transfer of the PGC. The 33 concatenated core genes of the PGC formed a robust phylogenetic tree and the comparison with single-gene trees demonstrated the dominance of joint evolution. The PGC tree is, however, largely incongruent with the species tree and at least seven transfers of the PGC are required to reconcile both phylogenies. The origin of a derived branch containing the PGC of the model organism Rhodobacter capsulatus correlates with a diagnostic gene replacement of pufC by pufX. The PGC is located on plasmids in six of the analyzed genomes and its DnaA-like replication module was discovered at a conserved central position of the PGC. A scenario of plasmid-borne horizontal transfer of the PGC and its reintegration into the chromosome could explain the current distribution of phototrophy in Rhodobacteraceae.
- MeSH
- fotosyntéza * MeSH
- fototrofní procesy MeSH
- fylogeneze MeSH
- genom bakteriální MeSH
- molekulární evoluce * MeSH
- multigenová rodina MeSH
- operon MeSH
- plazmidy genetika metabolismus MeSH
- přenos genů horizontální * MeSH
- replikace DNA MeSH
- Rhodobacteraceae klasifikace genetika metabolismus MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH