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.

Aarhus Institute of Advanced Studies Aarhus University Aarhus Denmark

Centre Algatech Institute of Microbiology CAS Třeboň Czechia

Department of Engineering Aarhus University Aarhus Denmark

Department of Environmental Science Aarhus University Roskilde Denmark

Department of Geography and Spatial Information Techniques Center for Land and Marine Spatial Utilization and Governance Research Ningbo University Ningbo China

The National Research Centre for the Working Environment Copenhagen Denmark

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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. 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. 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. 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 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. PubMed PMC

Chee-Sanford J., Tian D., Sanford R. (2019). Consumption of N2O and other N-cycle intermediates by 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. 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 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. 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. PubMed DOI PMC

Hanada S., Sekiguchi Y. (2014). “The phylum gemmatimonadetes,” in DOI

Hasholt B., Hagedorn B. (2000). Hydrology and geochemistry of river-borne material in a high arctic drainage system, Zackenberg, Northeast Greenland. 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. 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. PubMed PMC

Janssen P. H. (2006). Identifying the dominant soil bacterial taxa in libraries of 16S rRNA and 16S rRNA genes. 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. 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 PubMed DOI PMC

Katoh K., Standley D. M. (2013). MAFFT multiple sequence alignment software version 7: improvements in performance and usability. 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. PubMed DOI

Koblížek M. (2015). Ecology of aerobic anoxygenic phototrophs in aquatic environments. PubMed DOI

Koblížek M., Dachev M., Bína D., Nupur L., Piwosz K., Kaftan D. (2020). Utilization of light energy in phototrophic Gemmatimonadetes. 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. 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. PubMed DOI

Letunic I., Bork P. (2019). Interactive tree of life (iTOL) v4: recent updates and new developments. PubMed PMC

Lynch M. D., Neufeld J. D. (2015). Ecology and exploration of the rare biosphere. PubMed DOI

Nagashima S., Nagashima K. V. (2013). Comparison of photosynthesis gene clusters retrieved from total genome sequences of purple bacteria. DOI

Park D., Kim H., Yoon S. (2017). Nitrous oxide reduction by an obligate aerobic bacterium, 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. PubMed DOI

Pascual J., Foesel B. U., Geppert A., Huber K. J., Boedeker C., Luckner M., et al. (2018). PubMed DOI

Pascual J., Garcia-Lopez M., Bills G. F., Genilloud O. (2016). 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. PubMed DOI

Rosselló-Móra R., Amann R. (2015). Past and future species definitions for Bacteria and Archaea. PubMed DOI

Stamatakis A. (2014). RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. PubMed DOI PMC

Sullivan M. J., Petty N. K., Beatson S. A. (2011). Easyfig: a genome comparison visualizer. 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. 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. 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. 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. 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. PubMed DOI PMC

Woese C. R. (1987). Bacterial evolution. PubMed PMC

Youssef N. H., Elshahed M. S. (2009). Diversity rankings among bacterial lineages in soil. 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. 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. 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. PubMed DOI PMC

Zeng Y., Koblížek M. (2017). “Phototrophic Gemmatimonadetes: a new “purple” branch on the bacterial tree of life,” in DOI

Zeng Y., Selyanin V., Lukeš M., Dean J., Kaftan D., Feng F., et al. (2015). Characterization of the microaerophilic, bacteriochlorophyll a-containing bacterium 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 PubMed DOI PMC

Zhang H., Sekiguchi Y., Hanada S., Hugenholtz P., Kim H., Kamagata Y., et al. (2003). 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. PubMed PMC

Two solutions for efficient light-harvesting in phototrophic Gemmatimonadota

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Multi-environment ecogenomics analysis of the cosmopolitan phylum Gemmatimonadota

Diversity dynamics of aerobic anoxygenic phototrophic bacteria in a freshwater lake

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

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

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Phylum Gemmatimonadota and Its Role in the Environment

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

Characterization of the Aerobic Anoxygenic Phototrophic Bacterium Sphingomonas sp. AAP5

Common Presence of Phototrophic Gemmatimonadota in Temperate Freshwater Lakes