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Novel Acsf Gene Primers Revealed a Diverse Phototrophic Bacterial Population, Including Gemmatimonadetes, in Lake Taihu (China)

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Novel Acsf Gene Primers Revealed a Diverse Phototrophic Bacterial Population, Including Gemmatimonadetes, in Lake Taihu (China) University of Southern Denmark Novel acsF gene primers revealed a diverse phototrophic bacterial population, including Gemmatimonadetes, in Lake Taihu (China) Huang, Yili; Zeng, Yanhua; Lu, Hang; Feng, Hao; Zeng, Yonghui; Koblížek, Michal Published in: Applied and Environmental Microbiology DOI: 10.1128/AEM.01063-16 Publication date: 2016 Document version: Final published version Citation for pulished version (APA): Huang, Y., Zeng, Y., Lu, H., Feng, H., Zeng, Y., & Koblížek, M. (2016). Novel acsF gene primers revealed a diverse phototrophic bacterial population, including Gemmatimonadetes, in Lake Taihu (China). Applied and Environmental Microbiology, 82(18), 5587-5594. https://doi.org/10.1128/AEM.01063-16 Go to publication entry in University of Southern Denmark's Research Portal Terms of use This work is brought to you by the University of Southern Denmark. Unless otherwise specified it has been shared according to the terms for self-archiving. If no other license is stated, these terms apply: • You may download this work for personal use only. • You may not further distribute the material or use it for any profit-making activity or commercial gain • You may freely distribute the URL identifying this open access version If you believe that this document breaches copyright please contact us providing details and we will investigate your claim. Please direct all enquiries to [email protected] Download date: 26. Sep. 2021 crossmark Novel acsF Gene Primers Revealed a Diverse Phototrophic Bacterial Population, Including Gemmatimonadetes, in Lake Taihu (China) a a a a b c Yili Huang, Yanhua Zeng, Hang Lu, Hao Feng, Yonghui Zeng, Michal Koblížek Downloaded from Department of Environmental Science, College of Environmental and Resource Sciences, Zhejiang University, Hangzhou, Chinaa; Nordic Center for Earth Evolution and Institute of Biology, University of Southern Denmark, Odense, Denmarkb; Center Algatech, Institute of Microbiology CAS, Tøebonˇ, Czech Republicc ABSTRACT Anoxygenic phototrophs represent an environmentally important and phylogenetically diverse group of organisms. They har- vest light using bacteriochlorophyll-containing reaction centers. Recently, a novel phototrophic bacterium, Gemmatimonas phototrophica, belonging to a rarely studied phylum, Gemmatimonadetes, was isolated from a freshwater lake in the Gobi Des- ert. To obtain more information about the environmental distribution of phototrophic Gemmatimonadetes, we collected micro- http://aem.asm.org/ bial samples from the water column, upper sediment, and deeper anoxic sediment of Lake Taihu, China. MiSeq sequencing of the 16S rRNA, pufM, and bchY genes was carried out to assess the diversity of local phototrophic communities. In addition, we de- signed new degenerate primers of aerobic cyclase gene acsF, which serves as a convenient marker for both phototrophic Gemma- timonadetes and phototrophic Proteobacteria. Our results showed that most of the phototrophic species in Lake Taihu belong to Alpha- and Betaproteobacteria. Sequences of green sulfur and green nonsulfur bacteria (phototrophic Chlorobi and Chloroflexi, respectively) were found in the sediment. Using the newly designed primers, we identified a diverse community of phototrophic Gemmatimonadetes forming 30 operational taxonomic units. These species represented 10.5 and 17.3% of the acsF reads in the upper semiaerobic sediment and anoxic sediment, whereas their abundance in the water column was <1%. on August 17, 2017 by SYDDANSK UNIVERSITETSBIBLIOTEK IMPORTANCE Photosynthesis is one of the most fundamental biological processes on Earth. Recently, the presence of photosynthetic reaction centers has been reported from a rarely studied bacterial phylum, Gemmatimonadetes, but almost nothing is known about the diversity and environmental distribution of these organisms. The newly designed acsF primers were used to identify pho- totrophic Gemmatimonadetes from planktonic and sediment samples collected in Lake Taihu, China. The Gemmatimonadetes sequences were found mostly in the upper sediments, documenting the preference of Gemmatimonadetes for semiaerobic condi- tions. Our results also show that the phototrophic Gemmatimonadetes present in Lake Taihu were relatively diverse, encompass- ing 30 operational taxonomic units. hotosynthesis is one of the most important biological pro- as a phylogenetic marker indicated that phototrophic Gemmati- Pcesses on Earth. The ability of phototrophic organisms to uti- monadetes are distributed in various habitats such as fresh waters, lize sunlight provided an unlimited source of energy to sustain life sediments, estuarine waters, biofilms, plant surfaces, intertidal on our planet in all its abundance and complexity. The majority of sediment, soil, springs, and wastewater treatment plants, whereas photosynthetic organisms are formed by oxygenic species: plants, no sequences have been found in seawaters and marine sediments algae, and Cyanobacteria. Aside from these dominant organisms, (5). Gemmatimonadetes acsF-like sequences were found in the there exists a large variety of anoxygenic phototrophic (AP) bac- metagenome of the surface scum community that formed during teria that harvest light using various forms of bacteriochlorophyll. a cyanobacterial bloom in Lake Taihu, China (5), suggesting the The absorbed light is transferred into bacterial reaction centers, possible existence of phototrophic Gemmatimonadetes in this where it is used for primary photosynthetic reactions. AP species lake. have been found in seven bacterial phyla: Proteobacteria (purple Lake Taihu is a subtropical shallow (average depth, 2 m) fresh- anoxygenic phototrophs), Chlorobi (green sulfur bacteria), Chlo- roflexi (green nonsulfur bacteria), Firmicutes (heliobacteria), Aci- dobacteria, and Gemmatimonadetes (1, 2). Received 6 April 2016 Accepted 25 June 2016 The latest-found phylum, Gemmatimonadetes, contains only Accepted manuscript posted online 8 July 2016 one phototrophic species, i.e., Gemmatimonas phototrophica, Citation Huang Y, Zeng Y, Lu H, Feng H, Zeng Y, Koblížek M. 2016. Novel acsF which was isolated from a freshwater lake, Tia៮n É Hú, in the Gobi gene primers revealed a diverse phototrophic bacterial population, including desert (2). The new organism contains purple photosynthetic re- Gemmatimonadetes, in Lake Taihu (China). Appl Environ Microbiol 82:5587–5594. action centers but does not fix inorganic carbon (3). The environ- doi:10.1128/AEM.01063-16. Editor: S.-J. Liu, Chinese Academy of Sciences mental distribution of the novel AP lineage is largely unknown. In Address correspondence to Yili Huang, [email protected], or general, the members of the Gemmatimonadetes phylum have Michal Koblížek, [email protected]. been identified in polar or alpine environments, soils, and sedi- Supplemental material for this article may be found at http://dx.doi.org/10.1128 ments (4), but it is not clear whether the phototrophic members of /AEM.01063-16. this group share the same distribution pattern. The performed Copyright © 2016, American Society for Microbiology. All Rights Reserved. metagenomics search using the aerobic oxidative cyclase gene acsF September 2016 Volume 82 Number 18 Applied and Environmental Microbiology aem.asm.org 5587 Huang et al. water lake, located in the Yangtze River delta. With its surface area Application of the primer to cultured species. The newly designed of 2,250 km2, it is the third largest lake in China. Here, we sought primers were first tested with cultured species. The cultures were grown, to investigate the diversity patterns of phototrophic Gemmati- and the DNA was isolated as described previously (3, 10). Six strains of monadetes and other phototrophic species in more detail. To de- phototrophic Proteobacteria (Rhodovulum sulfidophilum, Erythrobacter termine the preferred habitat of phototrophic Gemmatimon- sp. strain NAP1, Congregibacter litoralis, Hoeflea phototrophica, Rubrivi- adetes, we collected samples not only from the water column but vax gelatinosus, and Roseobacter sp. strain COL2P) and Gemmatimonas phototrophica were used as positive-control samples. Heterotrophic Gem- also from the upper and deeper sediments. The bacterial commu- matimonas aurantiaca and the purple bacterium Rhodospirillum rubrum Downloaded from nity was characterized by deep sequencing of the 16S rRNA gene were used as negative controls. The PCR was carried out in 25 ␮lof amplicon. To specifically target the phototrophic organisms, we reaction mixture containing 20 ng of genomic DNA, 50 nM concentra- used two commonly used markers: the pufM gene encoding the M tions of degenerate primers,1UofTaq DNA polymerase (TaKaRa, subunit of the bacterial reaction centers (6) and the bchY gene China), 0.25 mM deoxynucleoside triphosphates (dNTPs), and PCR buf- encoding the chlorophyllide reductase subunit Y (7). The pufM fer. The PCR program was as follows: 94°C for 5 min, followed by 35 cycles gene has been applied in a number of environmental studies (8). of 94°C for 30 s, using a gradient from 45 to 60°C with six intervals for 45 Unfortunately, the commonly used primers usually only target s and 72°C for 1 min, followed in turn by a final extension at 72°C for 5 min. To verify the effectiveness of the primers, PCR products were gel phototrophic Proteobacteria, whereas the pufM sequences of other http://aem.asm.org/ AP phyla are not amplified. The newly introduced marker bchY purified and cloned into a pMD19-T vector (TaKaRa) according to the manufacturer’s instructions, followed by
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