Nejvíce citovaný článek - PubMed ID 27401973
Novel acsF Gene Primers Revealed a Diverse Phototrophic Bacterial Population, Including Gemmatimonadetes, in Lake Taihu (China)
UNLABELLED: The first phototrophic member of the bacterial phylum Gemmatimonadota, Gemmatimonas phototrophica AP64T, received all its photosynthesis genes via distant horizontal gene transfer from a purple bacterium. Here, we investigated how these acquired genes, which are tightly controlled by oxygen and light in the ancestor, are integrated into the regulatory system of its new host. G. phototrophica grew well under aerobic and semiaerobic conditions, with almost no difference in gene expression. Under aerobic conditions, the growth of G. phototrophica was optimal at 80 µmol photon m-2 s-1, while higher light intensities had an inhibitory effect. The transcriptome showed only a minimal response to the dark-light shift at optimal light intensity, while the exposure to a higher light intensity (200 µmol photon m-2 s-1) induced already stronger but still transient changes in gene expression. Interestingly, a singlet oxygen defense was not activated under any conditions tested. Our results indicate that G. phototrophica possesses neither the oxygen-dependent repression of photosynthesis genes known from purple bacteria nor the light-dependent repression described in aerobic anoxygenic phototrophs. Instead, G. phototrophica has evolved as a low-light species preferring reduced oxygen concentrations. Under these conditions, the bacterium can safely employ its photoheterotrophic metabolism without the need for complex regulatory mechanisms. IMPORTANCE: Horizontal gene transfer is one of the main mechanisms by which bacteria acquire new genes. However, it represents only the first step as the transferred genes have also to be functionally and regulatory integrated into the recipient's cellular machinery. Gemmatimonas phototrophica, a member of bacterial phylum Gemmatimonadota, acquired its photosynthesis genes via distant horizontal gene transfer from a purple bacterium. Thus, it represents a unique natural experiment, in which the entire package of photosynthesis genes was transplanted into a distant host. We show that G. phototrophica lacks the regulation of photosynthesis gene expressions in response to oxygen concentration and light intensity that are common in purple bacteria. This restricts its growth to low-light habitats with reduced oxygen. Understanding the regulation of horizontally transferred genes is important not only for microbial evolution but also for synthetic biology and the engineering of novel organisms, as these rely on the successful integration of foreign genes.
- Klíčová slova
- Gemmatimonadota, anoxygenic photosynthesis, bacteriochlorophyll, horizontal gene transfer, transcriptomics,
- MeSH
- bakteriální proteiny genetika metabolismus MeSH
- fotosyntéza * genetika MeSH
- přenos genů horizontální * MeSH
- regulace genové exprese u bakterií * účinky záření MeSH
- světlo MeSH
- transkriptom MeSH
- Publikační typ
- časopisecké články MeSH
- Názvy látek
- bakteriální proteiny MeSH
Bacteria are an important part of every ecosystem that they inhabit on Earth. Environmental microbiologists usually focus on a few dominant bacterial groups, neglecting less abundant ones, which collectively make up most of the microbial diversity. One of such less-studied phyla is Gemmatimonadota. Currently, the phylum contains only six cultured species. However, data from culture-independent studies indicate that members of Gemmatimonadota are common in diverse habitats. They are abundant in soils, where they seem to be frequently associated with plants and the rhizosphere. Moreover, Gemmatimonadota were found in aquatic environments, such as freshwaters, wastewater treatment plants, biofilms, and sediments. An important discovery was the identification of purple bacterial reaction centers and anoxygenic photosynthesis in this phylum, genes for which were likely acquired via horizontal gene transfer. So far, the capacity for anoxygenic photosynthesis has been described for two cultured species: Gemmatimonas phototrophica and Gemmatimonas groenlandica. Moreover, analyses of metagenome-assembled genomes indicate that it is also common in uncultured lineages of Gemmatimonadota. This review summarizes the current knowledge about this understudied bacterial phylum with an emphasis on its environmental distribution.
- Klíčová slova
- Gemmatimonadetes, Gemmatimonadota, MAGs, anoxygenic photosynthesis, photosynthetic gene cluster,
- Publikační typ
- časopisecké články MeSH
- přehledy MeSH
Members of the bacterial phylum Gemmatimonadota are ubiquitous in most natural environments and represent one of the top 10 most abundant bacterial phyla in soil. Sequences affiliated with Gemmatimonadota were also reported from diverse aquatic habitats; however, it remains unknown whether they are native organisms or represent bacteria passively transported from sediment or soil. To address this question, we analyzed metagenomes constructed from five freshwater lakes in central Europe. Based on the 16S rRNA gene frequency, Gemmatimonadota represented from 0.02 to 0.6% of all bacteria in the epilimnion and between 0.1 and 1% in the hypolimnion. These proportions were independently confirmed using catalyzed reporter deposition-fluorescence in situ hybridization (CARD-FISH). Some cells in the epilimnion were attached to diatoms (Fragilaria sp.) or cyanobacteria (Microcystis sp.), which suggests a close association with phytoplankton. In addition, we reconstructed 45 metagenome-assembled genomes (MAGs) related to Gemmatimonadota They represent several novel lineages, which persist in the studied lakes during the seasons. Three lineages contained photosynthesis gene clusters. One of these lineages was related to Gemmatimonas phototrophica and represented the majority of Gemmatimonadota retrieved from the lakes' epilimnion. The other two lineages came from hypolimnion and probably represented novel photoheterotrophic genera. None of these phototrophic MAGs contained genes for carbon fixation. Since most of the identified MAGs were present during the whole year and cells associated with phytoplankton were observed, we conclude that they represent truly limnic Gemmatimonadota distinct from the previously described species isolated from soils or sediments.IMPORTANCE Photoheterotrophic bacterial phyla such as Gemmatimonadota are key components of many natural environments. Its first photoheterotrophic cultured member, Gemmatimonas phototrophica, was isolated in 2014 from a shallow lake in the Gobi Desert. It contains a unique type of photosynthetic complex encoded by a set of genes which were likely received via horizontal transfer from Proteobacteria We were intrigued to discover how widespread this group is in the natural environment. In the presented study, we analyzed 45 metagenome-assembled genomes (MAGs) that were obtained from five freshwater lakes in Switzerland and Czechia. Interestingly, it was found that phototrophic Gemmatimonadota are relatively common in euphotic zones of the studied lakes, whereas heterotrophic Gemmatimonadota prevail in deeper waters. Moreover, our analysis of the MAGs documented that these freshwater species contain almost the same set of photosynthesis genes identified before in Gemmatimonas phototrophica originating from the Gobi Desert.
- Klíčová slova
- CARD-FISH, Gemmatimonadetes, Gemmatimonadota, MAGs, anoxygenic phototrophs, aquatic bacteria, freshwater ecology, metagenome, photosynthesis gene cluster,
- Publikační typ
- časopisecké články MeSH
The anoxygenic phototrophic bacteria (APB) are an active component of aquatic microbial communities. While DNA-based studies have delivered a detailed picture of APB diversity, they cannot provide any information on the activity of individual species. Therefore, we focused on the expression of a photosynthetic gene by APB communities in two freshwater lakes (Cep lake and the Římov Reservoir) in the Czech Republic. First, we analyzed expression levels of pufM during the diel cycle using RT-qPCR. The transcription underwent a strong diel cycle and was inhibited during the day in both lakes. Then, we compared DNA- (total) and RNA-based (active) community composition by sequencing pufM amplicon libraries. We observed large differences in expression activity among different APB phylogroups. While the total APB community in the Římov Reservoir was dominated by Betaproteobacteria, Alphaproteobacteria prevailed in the active library. A different situation was encountered in the oligotrophic lake Cep where Betaproteobacteria (order Burkholderiales) dominated both the DNA and RNA libraries. Interestingly, in Cep lake we found smaller amounts of highly active uncultured phototrophic Chloroflexi, as well as phototrophic Gemmatimonadetes. Despite the large diversity of APB communities, light repression of pufM expression seems to be a common feature of all aerobic APB present in the studied lakes.
- MeSH
- Alphaproteobacteria izolace a purifikace fyziologie účinky záření MeSH
- bakteriální proteiny genetika metabolismus MeSH
- Betaproteobacteria izolace a purifikace fyziologie účinky záření MeSH
- DNA bakterií genetika izolace a purifikace MeSH
- fotoperioda * MeSH
- fotosyntetická reakční centra (proteinové komplexy) genetika metabolismus MeSH
- fototrofní procesy genetika účinky záření MeSH
- fylogeneze MeSH
- jezera mikrobiologie MeSH
- mikrobiota fyziologie účinky záření MeSH
- regulace genové exprese u bakterií fyziologie účinky záření MeSH
- světlo škodlivé účinky MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Geografické názvy
- Česká republika MeSH
- Názvy látek
- bakteriální proteiny MeSH
- DNA bakterií MeSH
- fotosyntetická reakční centra (proteinové komplexy) MeSH
- PufM protein, Bacteria MeSH Prohlížeč
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
The growth rate is a fundamental characteristic of bacterial species, determining its contributions to the microbial community and carbon flow. High-throughput sequencing can reveal bacterial diversity, but its quantitative inaccuracy precludes estimation of abundances and growth rates from the read numbers. Here, we overcame this limitation by normalizing Illumina-derived amplicon reads using an internal standard: a constant amount of Escherichia coli cells added to samples just before biomass collection. This approach made it possible to reconstruct growth curves for 319 individual OTUs during the grazer-removal experiment conducted in a freshwater reservoir Římov. The high resolution data signalize significant functional heterogeneity inside the commonly investigated bacterial groups. For instance, many Actinobacterial phylotypes, a group considered to harbor slow-growing defense specialists, grew rapidly upon grazers' removal, demonstrating their considerable importance in carbon flow through food webs, while most Verrucomicrobial phylotypes were particle associated. Such differences indicate distinct life strategies and roles in food webs of specific bacterial phylotypes and groups. The impact of grazers on the specific growth rate distributions supports the hypothesis that bacterivory reduces competition and allows existence of diverse bacterial communities. It suggests that the community changes were driven mainly by abundant, fast, or moderately growing, and not by rare fast growing, phylotypes. We believe amplicon read normalization using internal standard (ARNIS) can shed new light on in situ growth dynamics of both abundant and rare bacteria.
