Nejvíce citovaný článek - PubMed ID 19949940
On the photosynthetic properties of marine bacterium COL2P belonging to Roseobacter clade
Aerobic anoxygenic phototrophic (AAP) bacteria are an important component of freshwater bacterioplankton. They can support their heterotrophic metabolism with energy from light, enhancing their growth efficiency. Based on results from cultures, it was hypothesized that photoheterotrophy provides an advantage under carbon limitation and facilitates access to recalcitrant or low-energy carbon sources. However, verification of these hypotheses for natural AAP communities has been lacking. Here, we conducted whole community manipulation experiments and compared the growth of AAP bacteria under carbon limited and with recalcitrant or low-energy carbon sources under dark and light (near-infrared light, λ > 800 nm) conditions to elucidate how they profit from photoheterotrophy. We found that AAP bacteria induce photoheterotrophic metabolism under carbon limitation, but they overcompete heterotrophic bacteria when carbon is available. This effect seems to be driven by physiological responses rather than changes at the community level. Interestingly, recalcitrant (lignin) or low-energy (acetate) carbon sources inhibited the growth of AAP bacteria, especially in light. This unexpected observation may have ecosystem-level consequences as lake browning continues. In general, our findings contribute to the understanding of the dynamics of AAP bacteria in pelagic environments.
- Klíčová slova
- acetate, aerobic anoxygenic phototrophic bacteria, carbon limitation, freshwater lakes, lignin, microbial ecology,
- MeSH
- aerobní bakterie metabolismus růst a vývoj MeSH
- Bacteria metabolismus růst a vývoj genetika MeSH
- ekosystém MeSH
- fototrofní procesy * MeSH
- heterotrofní procesy MeSH
- jezera mikrobiologie MeSH
- světlo MeSH
- uhlík * metabolismus MeSH
- Publikační typ
- časopisecké články MeSH
- Názvy látek
- uhlík * MeSH
Aerobic anoxygenic phototrophic (AAP) bacteria harvest light energy using bacteriochlorophyll-containing reaction centers to supplement their mostly heterotrophic metabolism. While their abundance and growth have been intensively studied in coastal environments, much less is known about their activity in oligotrophic open ocean regions. Therefore, we combined in situ sampling in the North Pacific Subtropical Gyre, north of O'ahu island, Hawaii, with two manipulation experiments. Infra-red epifluorescence microscopy documented that AAP bacteria represented approximately 2% of total bacteria in the euphotic zone with the maximum abundance in the upper 50 m. They conducted active photosynthetic electron transport with maximum rates up to 50 electrons per reaction center per second. The in situ decline of bacteriochlorophyll concentration over the daylight period, an estimate of loss rates due to predation, indicated that the AAP bacteria in the upper 50 m of the water column turned over at rates of 0.75-0.90 d-1. This corresponded well with the specific growth rate determined in dilution experiments where AAP bacteria grew at a rate 1.05 ± 0.09 d-1. An amendment of inorganic nitrogen to obtain N:P = 32 resulted in a more than 10 times increase in AAP abundance over 6 days. The presented data document that AAP bacteria are an active part of the bacterioplankton community in the oligotrophic North Pacific Subtropical Gyre and that their growth was mostly controlled by nitrogen availability and grazing pressure.IMPORTANCEMarine bacteria represent a complex assembly of species with different physiology, metabolism, and substrate preferences. We focus on a specific functional group of marine bacteria called aerobic anoxygenic phototrophs. These photoheterotrophic organisms require organic carbon substrates for growth, but they can also supplement their metabolic needs with light energy captured by bacteriochlorophyll. These bacteria have been intensively studied in coastal regions, but rather less is known about their distribution, growth, and mortality in the oligotrophic open ocean. Therefore, we conducted a suite of measurements in the North Pacific Subtropical Gyre to determine the distribution of these organisms in the water column and their growth and mortality rates. A nutrient amendment experiment showed that aerobic anoxygenic phototrophs were limited by inorganic nitrogen. Despite this, they grew more rapidly than average heterotrophic bacteria, but their growth was balanced by intense grazing pressure.
- Klíčová slova
- North Pacific Subtropical Gyre, Station ALOHA, aerobic anoxygenic phototrophs, bacteriochlorophyll a, marine bacteria,
- MeSH
- aerobní bakterie MeSH
- bakteriochlorofyly * metabolismus MeSH
- dusík metabolismus MeSH
- fototrofní procesy * MeSH
- mořská voda mikrobiologie MeSH
- voda metabolismus MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- bakteriochlorofyly * MeSH
- dusík MeSH
- voda 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 phototrophic (AAP) bacteria are a common component of freshwater microbial communities. They harvest light energy using bacteriochlorophyll a-containing reaction centers to supplement their predominantly heterotrophic metabolism. We used epifluorescence microscopy, HPLC, and infrared fluorometry to examine the dynamics of AAP bacteria in the mesotrophic lake Vlkov during the seasonal cycle. The mortality of AAP bacteria was estimated from diel changes of bacteriochlorophyll a fluorescence. The AAP abundance correlated with water temperature and DOC concentration. Its maximum was registered during late summer, when AAP bacteria made up 20% of total bacteria. The novel element of this study is the seasonal measurements of AAP mortality rates. The rates ranged between 1.15 and 4.56 per day with the maxima registered in early summer coinciding with the peak of primary production, which documents that AAP bacteria are a highly active component of freshwater microbial loop.
- MeSH
- aerobní bakterie klasifikace genetika izolace a purifikace účinky záření MeSH
- biodiverzita * MeSH
- fototrofní procesy MeSH
- jezera mikrobiologie MeSH
- kyslík metabolismus MeSH
- roční období MeSH
- světlo MeSH
- Publikační typ
- časopisecké články MeSH
- Názvy látek
- kyslík MeSH
Aerobic anoxygenic phototrophs (AAPs) are photoheterotrophic prokaryotes that are widespread in many limnic and marine environments. So far, little is known about their distribution in peat-bog lakes. Seventeen peat-bog lakes were sampled during three summer seasons 2009, 2011, and 2012, and the vertical distribution of AAPs was determined by infrared epifluorescence microscopy. The analysis demonstrated that in the surface layers of the studied lakes, AAP abundance ranged from 0.3 to 12.04 × 10(5) cells mL(-1), which represents <1 to 18.3 % of the total bacteria. The vertical distribution of AAPs confirmed their presence in the upper parts of the water column with minimum numbers in the anoxic bottom waters. We have shown that the AAP abundance was significantly positively correlated with the water pH, and the highest proportion of photoheterotrophs was found in peat-bog lakes with a pH between 6.7 and 7.6. Our results demonstrated an influence of water acidity on the abundance of AAPs, which may reflect a fundamental difference in the microbial composition between acidic and pH neutral peat-bog lakes.
- Klíčová slova
- Aerobic anoxygenic phototrophic bacteria, Environmental factors, Humic and dystrophic lakes, Peat-bog lakes, pH,
- MeSH
- aerobní bakterie fyziologie MeSH
- jezera mikrobiologie MeSH
- kyslík MeSH
- mikrobiologie vody MeSH
- mokřady * MeSH
- monitorování životního prostředí MeSH
- půda * MeSH
- roční období MeSH
- Publikační typ
- časopisecké články MeSH
- Názvy látek
- kyslík MeSH
- půda * MeSH
Light-harvesting capacity was investigated in six species of aerobic anoxygenic phototrophic (AAP) bacteria using absorption spectroscopy, fluorescence emission spectroscopy, and pigment analyses. Aerobically grown AAP cells contained approx. 140-1800 photosynthetic reaction centers per cell, an order of magnitude less than purple non-sulfur bacteria grown semiaerobically. Three of the studied AAP species did not contain outer light-harvesting complexes, and the size of their reaction center core complexes (RC-LH1 core complexes) varied between 29 and 36 bacteriochlorophyll molecules. In AAP species containing accessory antennae, the size was frequently reduced, providing between 5 and 60 additional bacteriochlorophyll molecules. In Roseobacter litoralis, it was found that cells grown at a higher light intensity contained more reaction centers per cell, while the size of the light-harvesting complexes was reduced. The presented results document that AAP species have both the reduced number and size of light-harvesting complexes which is consistent with the auxiliary role of phototrophy in this bacterial group.
- Klíčová slova
- Bacterial photosynthesis, Bacteriochlorophyll, Photosynthetic unit size, Purple non-sulfur bacteria, Reaction center core complex,
- MeSH
- aerobióza MeSH
- Alphaproteobacteria chemie metabolismus MeSH
- bakteriochlorofyly metabolismus MeSH
- fotosyntetická reakční centra (proteinové komplexy) chemie metabolismus MeSH
- fototrofní procesy MeSH
- Gammaproteobacteria chemie metabolismus MeSH
- světlosběrné proteinové komplexy chemie metabolismus MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- bakteriochlorofyly MeSH
- fotosyntetická reakční centra (proteinové komplexy) MeSH
- světlosběrné proteinové komplexy MeSH
The Roseobacter clade represents one of the most important bacterial groups in marine environments. While some of its members are heterotrophs, many Roseobacter clade members contain bacterial photosynthetic reaction centers. We investigated the phylogeny of pufL and pufM genes encoding the L and M subunits of reaction centers using available genomic data and our own cultured species. Interestingly, phylogeny of pufL and pufM genes largely deviated from 16S rRNA-based phylogeny. The sequences split into two clearly distinct clades. While most of the studied species contained pufL and pufM sequences related to those found in Roseobacter litoralis, some of the marine species contained sequences related to the freshwater Rhodobacter species. In addition, genomic data documents that Roseobacter-type centers contain cytochrome c subunits (pufC gene product), whereas Rhodobacter-type centers incorporate PufX proteins. This indicates that the two forms of the reaction centers are not only distinct phylogenetically, but also structurally. The large deviation of pufL and pufM phylogeny from 16S phylogeny indicates multiple horizontal transfers of the puf operon among members of the order Rhodobacterales.
- MeSH
- bakteriální proteiny genetika metabolismus MeSH
- fototrofní procesy MeSH
- fylogeneze MeSH
- molekulární sekvence - údaje MeSH
- operon * MeSH
- přenos genů horizontální * MeSH
- Roseobacter klasifikace genetika metabolismus MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- bakteriální proteiny MeSH
Photosynthetic bacteria emerged on Earth more than 3 Gyr ago. To date, despite a long evolutionary history, species containing (bacterio)chlorophyll-based reaction centers have been reported in only 6 out of more than 30 formally described bacterial phyla: Cyanobacteria, Proteobacteria, Chlorobi, Chloroflexi, Firmicutes, and Acidobacteria. Here we describe a bacteriochlorophyll a-producing isolate AP64 that belongs to the poorly characterized phylum Gemmatimonadetes. This red-pigmented semiaerobic strain was isolated from a freshwater lake in the western Gobi Desert. It contains fully functional type 2 (pheophytin-quinone) photosynthetic reaction centers but does not assimilate inorganic carbon, suggesting that it performs a photoheterotrophic lifestyle. Full genome sequencing revealed the presence of a 42.3-kb-long photosynthesis gene cluster (PGC) in its genome. The organization and phylogeny of its photosynthesis genes suggests an ancient acquisition of PGC via horizontal transfer from purple phototrophic bacteria. The data presented here document that Gemmatimonadetes is the seventh bacterial phylum containing (bacterio)chlorophyll-based phototrophic species. To our knowledge, these data provide the first evidence that (bacterio)chlorophyll-based phototrophy can be transferred between distant bacterial phyla, providing new insights into the evolution of bacterial photosynthesis.
- Klíčová slova
- aerobic photoheterotroph, anoxygenic photosynthesis, bacterial pigments, fluorescence imaging system, horizontal gene transfer,
- MeSH
- Bacteria cytologie genetika metabolismus MeSH
- druhová specificita MeSH
- fluorescenční mikroskopie MeSH
- fluorometrie MeSH
- fotosystém II (proteinový komplex) genetika metabolismus MeSH
- fylogeneze * MeSH
- jezera mikrobiologie MeSH
- modely genetické MeSH
- molekulární sekvence - údaje MeSH
- pravděpodobnostní funkce MeSH
- RNA ribozomální 16S genetika MeSH
- sekvence nukleotidů MeSH
- sekvenční analýza DNA MeSH
- shluková analýza MeSH
- spektrální analýza MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Geografické názvy
- Čína MeSH
- Názvy látek
- fotosystém II (proteinový komplex) MeSH
- RNA ribozomální 16S MeSH
Magnesium-protoporphyrin IX monomethylester cyclase is one of the key enzymes of the bacteriochlorophyll biosynthesis pathway. There exist two fundamentally different forms of this enzyme. The oxygen-dependent form, encoded by the gene acsF, catalyzes the formation of the bacteriochlorophyll fifth ring using oxygen, whereas the oxygen-independent form encoded by the gene bchE utilizes an oxygen atom extracted from water. The presence of acsF and bchE genes was surveyed in various phototrophic Proteobacteria using the available genomic data and newly designed degenerated primers. It was found that while the majority of purple nonsulfur bacteria contained both forms of the cyclase, the purple sulfur bacteria contained only the oxygen-independent form. All tested species of aerobic anoxygenic phototrophs contained acsF genes, but some of them also retained the bchE gene. In contrast to bchE phylogeny, the acsF phylogeny was in good agreement with 16S inferred phylogeny. Moreover, the survey of the genome data documented that the acsF gene occupies a conserved position inside the photosynthesis gene cluster, whereas the bchE location in the genome varied largely between the species. This suggests that the oxygen-dependent cyclase was recruited by purple phototrophic bacteria very early during their evolution. The primary sequence and immunochemical similarity with its cyanobacterial counterparts suggests that acsF may have been acquired by Proteobacteria via horizontal gene transfer from cyanobacteria. The acquisition of the gene allowed purple nonsulfur phototrophic bacteria to proliferate in the mildly oxygenated conditions of the Proterozoic era.
- MeSH
- bakteriální proteiny analýza chemie genetika MeSH
- fotosyntéza genetika MeSH
- fylogeneze MeSH
- genom bakteriální MeSH
- kyslík metabolismus MeSH
- oxygenasy analýza chemie genetika MeSH
- protein - isoformy analýza chemie genetika MeSH
- Proteobacteria enzymologie genetika metabolismus MeSH
- sinice enzymologie genetika MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- bakteriální proteiny MeSH
- kyslík MeSH
- magnesium protoporphyrin monomethyl ester oxidative cyclase MeSH Prohlížeč
- oxygenasy MeSH
- protein - isoformy MeSH
Aerobic anoxygenic phototrophs contain photosynthetic reaction centers composed of bacteriochlorophyll. These organisms are photoheterotrophs, as they require organic carbon substrates for their growth whereas light-derived energy has only an auxiliary function. To establish the contribution of light energy to their metabolism, we grew the phototrophic strain Erythrobacter sp. NAP1 in a carbon-limited chemostat regimen on defined carbon sources (glutamate, pyruvate, acetate, and glucose) under conditions of different light intensities. When grown in a light-dark cycle, these bacteria accumulated 25% to 110% more biomass in terms of carbon than cultures grown in the dark. Cultures grown on glutamate accumulated the most biomass at moderate light intensities of 50 to 150 μmol m(-2) s(-1) but were inhibited at higher light intensities. In the case of pyruvate, we did not find any inhibition of growth by high irradiance. The extent of anaplerotic carbon fixation was detemined by radioactive bicarbonate incorporation assays. While the carboxylation activity provided 4% to 11% of the cellular carbon in the pyruvate-grown culture, in the glutamate-grown cells it provided only approximately 1% of the carbon. Additionally, we tested the effect of light on respiration and photosynthetic electron flow. With increasing light intensity, respiration decreased to approximately 25% of its dark value and was replaced by photophosphorylation. The additional energy from light allows the aerobic anoxygenic phototrophs to accumulate the supplied organic carbon which would otherwise be respired. The higher efficiency of organic carbon utilization may provide an important competitive advantage during growth under carbon-limited conditions.
- MeSH
- aerobióza MeSH
- biomasa MeSH
- fototrofní procesy * MeSH
- hydrogenuhličitany metabolismus MeSH
- izotopové značení MeSH
- izotopy uhlíku metabolismus MeSH
- koloběh uhlíku MeSH
- kultivační média chemie MeSH
- pyruváty metabolismus MeSH
- Sphingomonadaceae metabolismus účinky záření MeSH
- světlo * MeSH
- tma MeSH
- transport elektronů MeSH
- uhlík metabolismus MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- hydrogenuhličitany MeSH
- izotopy uhlíku MeSH
- kultivační média MeSH
- pyruváty MeSH
- uhlík MeSH