Gemmatimonas groenlandica sp. nov. Is an Aerobic Anoxygenic Phototroph in the Phylum Gemmatimonadetes

. 2020 ; 11 () : 606612. [epub] 20210115

Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic-ecollection

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid33519753

The bacterial phylum Gemmatimonadetes contains members capable of performing bacteriochlorophyll-based phototrophy (chlorophototrophy). However, only one strain of chlorophototrophic Gemmatimonadetes bacteria (CGB) has been isolated to date, hampering our further understanding of their photoheterotrophic lifestyle and the evolution of phototrophy in CGB. By combining a culturomics strategy with a rapid screening technique for chlorophototrophs, we report the isolation of a new member of CGB, Gemmatimonas (G.) groenlandica sp. nov., from the surface water of a stream in the Zackenberg Valley in High Arctic Greenland. Distinct from the microaerophilic G. phototrophica strain AP64T, G. groenlandica strain TET16T is a strictly aerobic anoxygenic phototroph, lacking many oxygen-independent enzymes while possessing an expanded arsenal for coping with oxidative stresses. Its pigment composition and infra-red absorption properties are also different from G. phototrophica, indicating that it possesses a different photosystem apparatus. The complete genome sequence of G. groenlandica reveals unique and conserved features in the photosynthesis gene clusters of CGB. We further analyzed metagenome-assembled genomes of CGB obtained from soil and glacier metagenomes from Northeast Greenland, revealing a wide distribution pattern of CGB beyond the stream water investigated.

Zobrazit více v PubMed

Asnicar F., Thomas A. M., Beghini F., Mengoni C., Manara S., Manghi P., et al. (2020). Precise phylogenetic analysis of microbial isolates and genomes from metagenomes using PhyloPhlAn 3.0. Nat. Commun. 11:2500. PubMed PMC

Aziz R. K., Bartels D., Best A. A., DeJongh M., Disz T., Edwards R. A., et al. (2008). The RAST server: rapid annotations using subsystems technology. BMC Genom. 9:75. 10.1186/1471-2164-9-75 PubMed DOI PMC

Battistuzzi F. U., Feijao A., Hedges S. B. (2004). A genomic timescale of prokaryote evolution: insights into the origin of methanogenesis, phototrophy, and the colonization of land. BMC Evol. Biol. 4:44. 10.1186/1471-2148-4-44 PubMed DOI PMC

Boldareva-Nuianzina E. N., Bláhová Z., Sobotka R., Koblížek M. (2013). Distribution and origin of oxygen-dependent and oxygen-independent forms of Mg-protoporphyrin monomethylester cyclase among phototrophic proteobacteria. Appl. Environ. Microbiol. 79 2596–2604. 10.1128/aem.00104-13 PubMed DOI PMC

Cabello-Yeves P. J., Zemskaya T. I., Rosselli R., Coutinho F. H., Zakharenko A. S., Blinov V. V., et al. (2018). Genomes of novel microbial lineages assembled from the sub-ice waters of Lake Baikal. Appl. Environ. Microbiol. 84:e02132-17. PubMed PMC

Chee-Sanford J., Tian D., Sanford R. (2019). Consumption of N2O and other N-cycle intermediates by Gemmatimonas aurantiaca strain T-27. Microbiol. SGM 165 1345–1354. 10.1099/mic.0.000847 PubMed DOI

Chun J., Oren A., Ventosa A., Christensen H., Arahal D. R., da Costa M. S., et al. (2018). Proposed minimal standards for the use of genome data for the taxonomy of prokaryotes. Int. J. Syst. Evol. Microbiol. 68 461–466. 10.1099/ijsem.0.002516 PubMed DOI

Dachev M., Bína D., Sobotka R., Moravcová L., Gardian Z., Kaftan D., et al. (2017). Unique double concentric ring organization of light harvesting complexes in Gemmatimonas phototrophica. PLoS Biol. 15:e2003943. 10.1371/journal.pbio.2003943 PubMed DOI PMC

Darriba D., Posada D., Kozlov A. M., Stamatakis A., Morel B., Flouri T. (2020). ModelTest-NG: a new and scalable tool for the selection of DNA and protein evolutionary models. Mol. Biol. Evol. 37 291–294. 10.1093/molbev/msz189 PubMed DOI PMC

DeBruyn J. M., Nixon L. T., Fawaz M. N., Johnson A. M., Radosevich M. (2011). Global biogeography and quantitative seasonal dynamics of gemmatimonadetes in soil. Appl. Environ. Microbiol. 77 6295–6300. 10.1128/aem.05005-11 PubMed DOI PMC

Hanada S., Sekiguchi Y. (2014). “The phylum gemmatimonadetes,” in The Prokaryotes – Other Major Lineages of Bacteria and the Archaea, eds Rosenberg E., DeLong E. F., Lory S., Stackebrandt E., Thompson F. (Berlin: Springer; ), 677–681. 10.1007/978-3-642-38954-2_164 DOI

Hasholt B., Hagedorn B. (2000). Hydrology and geochemistry of river-borne material in a high arctic drainage system, Zackenberg, Northeast Greenland. Arctic Antarct. Alpine Res. 32 84–94. 10.1080/15230430.2000.12003342 DOI

Jaffe A. L., Castelle C. J., Dupont C. L., Banfield J. F. (2019). Lateral gene transfer shapes the distribution of RuBisCO among candidate phyla radiation bacteria and DPANN archaea. Mol. Biol. Evol. 36 435–446. 10.1093/molbev/msy234 PubMed DOI PMC

Jain C., Rodriguez-R L. M., Phillippy A. M., Konstantinidis K. T., Aluru S. (2018). High throughput ANI analysis of 90K prokaryotic genomes reveals clear species boundaries. Nat. Commun. 9 1–8. PubMed PMC

Janssen P. H. (2006). Identifying the dominant soil bacterial taxa in libraries of 16S rRNA and 16S rRNA genes. Appl. Environ. Microbiol. 72 1719–1728. 10.1128/aem.72.3.1719-1728.2006 PubMed DOI PMC

Jousset A., Bienhold C., Chatzinotas A., Gallien L., Gobet A., Kurm V., et al. (2017). Where less may be more: how the rare biosphere pulls ecosystems strings. ISME J. 11 853–862. 10.1038/ismej.2016.174 PubMed DOI PMC

Kato K., Tanaka R., Sano S., Tanaka A., Hosaka H. (2010). Identification of a gene essential for protoporphyrinogen IX oxidase activity in the Cyanobacterium synechocystis sp. PCC6803. Proc. Natl. Acad. Sci. U.S.A. 107 16649–16654. 10.1073/pnas.1000771107 PubMed DOI PMC

Katoh K., Standley D. M. (2013). MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol. Biol. Evol. 30 772–780. 10.1093/molbev/mst010 PubMed DOI PMC

Kim M., Oh H. S., Park S. C., Chun J. (2014). Towards a taxonomic coherence between average nucleotide identity and 16S rRNA gene sequence similarity for species demarcation of prokaryotes. Int. J. Syst. Evol. Microbiol. 64 346–351. 10.1099/ijs.0.059774-0 PubMed DOI

Koblížek M. (2015). Ecology of aerobic anoxygenic phototrophs in aquatic environments. FEMS Microbiol. Rev. 39 854–870. 10.1093/femsre/fuv032 PubMed DOI

Koblížek M., Dachev M., Bína D., Nupur L., Piwosz K., Kaftan D. (2020). Utilization of light energy in phototrophic Gemmatimonadetes. J. Photochem. Photobiol. B. 213:112085. 10.1016/j.jphotobiol.2020.112085 PubMed DOI

Kozlov A. M., Darriba D., Flouri T., Morel B., Stamatakis A. (2019). RAxML-NG: a fast, scalable and user-friendly tool for maximum likelihood phylogenetic inference. Bioinformatics 35 4453–4455. 10.1093/bioinformatics/btz305 PubMed DOI PMC

Lagier J. C., Dubourg G., Million M., Cadoret F., Bilen M., Fenollar F., et al. (2018). Culturing the human microbiota and culturomics. Nat. Rev. Microbiol. 16 540–550. 10.1038/s41579-018-0041-0 PubMed DOI

Letunic I., Bork P. (2019). Interactive tree of life (iTOL) v4: recent updates and new developments. Nucleic Acids Res. 47 W256–W259. PubMed PMC

Lynch M. D., Neufeld J. D. (2015). Ecology and exploration of the rare biosphere. Nat. Rev. Microbiol. 13 217–229. 10.1038/nrmicro3400 PubMed DOI

Nagashima S., Nagashima K. V. (2013). Comparison of photosynthesis gene clusters retrieved from total genome sequences of purple bacteria. Adv. Bot. Res. 66 151–178. 10.1016/b978-0-12-397923-0.00005-9 DOI

Park D., Kim H., Yoon S. (2017). Nitrous oxide reduction by an obligate aerobic bacterium, Gemmatimonas aurantiaca strain T-27. Appl. Environ. Microbiol. 83 e502–e517. PubMed PMC

Parks D. H., Chuvochina M., Waite D. W., Rinke C., Skarshewski A., Chaumeil P. A., et al. (2018). A standardized bacterial taxonomy based on genome phylogeny substantially revises the tree of life. Nat. Biotechnol. 36 996–1004. 10.1038/nbt.4229 PubMed DOI

Pascual J., Foesel B. U., Geppert A., Huber K. J., Boedeker C., Luckner M., et al. (2018). Roseisolibacter agri gen. nov., sp nov., a novel slow-growing member of the under-represented phylum Gemmatimonadetes. Intern. J. Syst. Evol. Microbiol. 68 1028–1036. 10.1099/ijsem.0.002619 PubMed DOI

Pascual J., Garcia-Lopez M., Bills G. F., Genilloud O. (2016). Longimicrobium terrae gen. nov., sp nov., an Oligotrophic bacterium of the under-represented phylum Gemmatimonadetes isolated through a system of miniaturized diffusion chambers. Intern. J. Syst. Evol. Microbiol. 66 1976–1985. 10.1099/ijsem.0.000974 PubMed DOI

Pastor A., Freixa A., Skovsholt L. J., Wu N., Romaní A. M., Riis T. (2019). Microbial organic matter utilization in high-arctic streams: key enzymatic controls. Microb. Ecol. 78 539–554. 10.1007/s00248-019-01330-w PubMed DOI

Rosselló-Móra R., Amann R. (2015). Past and future species definitions for Bacteria and Archaea. Syst. Appl. Microbiol. 38 209–216. 10.1016/j.syapm.2015.02.001 PubMed DOI

Stamatakis A. (2014). RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30 1312–1313. 10.1093/bioinformatics/btu033 PubMed DOI PMC

Sullivan M. J., Petty N. K., Beatson S. A. (2011). Easyfig: a genome comparison visualizer. Bioinformatics 27 1009–1010. 10.1093/bioinformatics/btr039 PubMed DOI PMC

Tabita F. R., Hanson T. E., Li H., Satagopan S., Singh J., Chan S. (2007). Function, structure, and evolution of the RubisCO-like proteins and their RubisCO homologs. Microbiol. Mol. Biol. Rev. 71 576–599. 10.1128/mmbr.00015-07 PubMed DOI PMC

Tahon G., Willems A. (2017). Isolation and characterization of aerobic anoxygenic phototrophs from exposed soils from the Sof. Rondane Mountains, East Antarctica. Syst. Appl. Microbiol. 40 357–369. 10.1016/j.syapm.2017.05.007 PubMed DOI

Vavourakis C. D., Mehrshad M., Balkema C., Van Hall R., Andrei A. Ş., Ghai R., et al. (2019). Metagenomes and metatranscriptomes shed new light on the microbial-mediated sulfur cycle in a Siberian soda lake. BMC Biol. 17:69. 10.1186/s12915-019-0688-7 PubMed DOI PMC

Wick R. R., Judd L. M., Gorrie C. L., Holt K. E. (2017). Unicycler: resolving bacterial genome assemblies from short and long sequencing reads. PLoS Comput. Biol. 13:e1005595. 10.1371/journal.pcbi.1005595 PubMed DOI PMC

Wilke A., Bischof J., Gerlach W., Glass E., Harrison T., Keegan K. P., et al. (2016). The MG-RAST metagenomics database and portal in 2015. Nucleic Acids Res. 44 D590–D594. 10.1007/8623_2015_119 PubMed DOI PMC

Woese C. R. (1987). Bacterial evolution. Microbiol. Rev. 51:221. PubMed PMC

Youssef N. H., Elshahed M. S. (2009). Diversity rankings among bacterial lineages in soil. ISME J. 3 305–313. 10.1038/ismej.2008.106 PubMed DOI

Zeng Y., Baumbach J., Barbosa E. G. V., Azevedo V., Zhang C., Koblížek M. (2016). Metagenomic evidence for the presence of phototrophic Gemmatimonadetes bacteria in diverse environments. Environ. Microbiol. Rep. 8 139–149. 10.1111/1758-2229.12363 PubMed DOI

Zeng Y., Chen H., Madsen A. M., Zervas A., Nielsen T. K., Andrei A., et al. (2020). Potential rhodopsin and bacteriochlorophyll-based dual phototrophy in a high Arctic glacier. mBio 11:e02641-20. 10.1128/mBio.02641-20 PubMed DOI PMC

Zeng Y., Feng F., Medová H., Dean J., Koblížek M. (2014). Functional type 2 photosynthetic reaction centers found in the rare bacterial phylum Gemmatimonadetes. Proc. Natl. Acad. Sci. U.S.A. 111 7795–7800. 10.1073/pnas.1400295111 PubMed DOI PMC

Zeng Y., Koblížek M. (2017). “Phototrophic Gemmatimonadetes: a new “purple” branch on the bacterial tree of life,” in Modern Topics in the Phototrophic Prokaryotes, ed. Hallenbeck P. C. (Cham: Springer; ), 163–192. 10.1007/978-3-319-46261-5_5 DOI

Zeng Y., Selyanin V., Lukeš M., Dean J., Kaftan D., Feng F., et al. (2015). Characterization of the microaerophilic, bacteriochlorophyll a-containing bacterium Gemmatimonas phototrophica sp. nov., and emended descriptions of the genus Gemmatimonas and Gemmatimonas aurantiaca. Intern. J. Syst. Evol. Microbiol. 65 2410–2419. 10.1099/ijs.0.000272 PubMed DOI

Zervas A., Zeng Y., Madsen A. M., Hansen L. H. (2019). Genomics of aerobic photoheterotrophs in wheat phyllosphere reveals divergent evolutionary patterns of photosynthetic genes in Methylobacterium spp. Genome Biol. Evol. 11 2895–2908. 10.1093/gbe/evz204 PubMed DOI PMC

Zhang H., Sekiguchi Y., Hanada S., Hugenholtz P., Kim H., Kamagata Y., et al. (2003). Gemmatimonas aurantiaca gen. nov., sp nov., a gram-negative, aerobic, polyphosphate-accumulating micro-organism, the first cultured representative of the new bacterial phylum Gemmatimonadetes phyl. nov. Intern. J. Syst. Evol. Microbiol. 53 1155–1163. 10.1099/ijs.0.02520-0 PubMed DOI

Zorz J. K., Sharp C., Kleiner M., Gordon P. M., Pon R.T., Dong X., et al. (2019). A shared core microbiome in soda lakes separated by large distances. Nat. Commun. 10 1–10. PubMed PMC

Nejnovějších 20 citací...

Zobrazit více v
Medvik | PubMed

Minimal transcriptional regulation of horizontally transferred photosynthesis genes in phototrophic bacterium Gemmatimonas phototrophica

. 2024 Sep 17 ; 9 (9) : e0070624. [epub] 20240827

Multi-environment ecogenomics analysis of the cosmopolitan phylum Gemmatimonadota

. 2023 Sep 21 ; 11 (5) : e0111223. [epub] 20230921

Diversity dynamics of aerobic anoxygenic phototrophic bacteria in a freshwater lake

. 2023 Feb ; 15 (1) : 60-71. [epub] 20221212

The Influence of Calcium on the Growth, Morphology and Gene Regulation in Gemmatimonas phototrophica

. 2022 Dec 22 ; 11 (1) : . [epub] 20221222

Atmospheric chemosynthesis is phylogenetically and geographically widespread and contributes significantly to carbon fixation throughout cold deserts

. 2022 Nov ; 16 (11) : 2547-2560. [epub] 20220806

2.4-Å structure of the double-ring Gemmatimonas phototrophica photosystem

. 2022 Feb 18 ; 8 (7) : eabk3139. [epub] 20220216

Phylum Gemmatimonadota and Its Role in the Environment

. 2022 Jan 12 ; 10 (1) : . [epub] 20220112

Structure elucidation of the novel carotenoid gemmatoxanthin from the photosynthetic complex of Gemmatimonas phototrophica AP64

. 2021 Aug 05 ; 11 (1) : 15964. [epub] 20210805

Characterization of the Aerobic Anoxygenic Phototrophic Bacterium Sphingomonas sp. AAP5

. 2021 Apr 06 ; 9 (4) : . [epub] 20210406

Common Presence of Phototrophic Gemmatimonadota in Temperate Freshwater Lakes

. 2021 Mar 16 ; 6 (2) : . [epub] 20210316

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...