A new symbiotic nanoarchaeote (Candidatus Nanoclepta minutus) and its host (Zestosphaera tikiterensis gen. nov., sp. nov.) from a New Zealand hot spring

Emily St. John, Yitai Liu, Mircea Podar, Matthew B. Stott, Jennifer Meneghin, Zhiqiang Chen, Kirill Lagutin, Kevin Mitchell, Anna Louise Reysenbach

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46 Scopus citations

Abstract

Three thermophilic Nanoarchaeota-Crenarchaeota symbiotic systems have been described. We obtained another stable anaerobic enrichment culture at 80 °C, pH 6.0 from a New Zealand hot spring. The nanoarchaeote (Ncl-1) and its host (NZ3T) were isolated in co-culture and their genomes assembled. The small (∼200 nm) flagellated cocci were often attached to larger cocci. Based on 16S rRNA gene similarity (88.4%) and average amino acid identity (52%), Ncl-1 is closely related to Candidatus Nanopusillus acidilobi. Their genomes both encode for archaeal flagella and partial glycolysis and gluconeogenesis pathways, but lack ATP synthase genes. Like Nanoarchaeum equitans, Ncl-1 has a CRISPR-Cas system. Ncl-1 also relies on its crenarchaeotal host for most of its biosynthetic needs. The host NZ3T was isolated and grows on proteinaceous substrates but not on sugars, alcohols, or fatty acids. NZ3T requires thiosulfate and grows best at 82 °C, pH 6.0. NZ3T is most closely related to the Desulfurococcaceae, Ignisphaera aggregans (∼92% 16S rRNA gene sequence similarity, 45% AAI). Based on phylogenetic, physiological and genomic data, Ncl-1 and NZ3T represent novel genera in the Nanoarchaeota and the Desulfurococcaceae, respectively, with the proposed names Candidatus Nanoclepta minutus and Zestosphaera tikiterensis gen. nov., sp. nov., type strain NZ3T (=DSMZ 107634T = OCM 1213T).

Original languageEnglish
Pages (from-to)94-106
Number of pages13
JournalSystematic and Applied Microbiology
Volume42
Issue number1
DOIs
StatePublished - Jan 2019

Funding

We would like to thank Dr. Aharon Oren for providing correct etymology for our novel taxa, Dr. Kenneth Stedman for initial help with TEM, Dr. Richard Davis, John Donaho and Nicole Wagner for assistance in the bioinformatics, Kristen Brileya for developing the qPCR primers, Kira Makarova for guidance with protein annotation, and Stefan L’Haridon for many helpful discussions. We also thank Steve Allman, Zamin Yang and Dawn Klingeman from Oak Ridge National Laboratory (ORNL) for assistance with cell sorting, molecular biology techniques and MiSeq sequencing. ORNL is managed by UT-Battelle, LLC, for the U.S. Department of Energy under contract DE-AC05-00OR22725. This research was funded through grants from the National Science Foundation ( DEB-1134877 ), the National Aeronautics and Space Administration ( NNX16AJ66G ), and the Geothermal Resources of New Zealand (GRN) Program at GNS Science . We acknowledge and thank Tikitere Trust for their enthusiasm for our research and assistance in access and sampling of the Hell’s Gate geothermal features. TEM data acquisition was performed at the Portland State University Center for Electron Microscopy and Nanofabrication (CEMN), which is generously supported by the NSF, Murdoch Charitable Trust, ONAMI, and FEI (currently Thermo Fisher Scientific). We would like to thank Dr. Aharon Oren for providing correct etymology for our novel taxa, Dr. Kenneth Stedman for initial help with TEM, Dr. Richard Davis, John Donaho and Nicole Wagner for assistance in the bioinformatics, Kristen Brileya for developing the qPCR primers, Kira Makarova for guidance with protein annotation, and Stefan L'Haridon for many helpful discussions. We also thank Steve Allman, Zamin Yang and Dawn Klingeman from Oak Ridge National Laboratory (ORNL) for assistance with cell sorting, molecular biology techniques and MiSeq sequencing. ORNL is managed by UT-Battelle, LLC, for the U.S. Department of Energy under contract DE-AC05-00OR22725. This research was funded through grants from the National Science Foundation (DEB-1134877), the National Aeronautics and Space Administration (NNX16AJ66G), and the Geothermal Resources of New Zealand (GRN) Program at GNS Science. We acknowledge and thank Tikitere Trust for their enthusiasm for our research and assistance in access and sampling of the Hell's Gate geothermal features. TEM data acquisition was performed at the Portland State University Center for Electron Microscopy and Nanofabrication (CEMN), which is generously supported by the NSF, Murdoch Charitable Trust, ONAMI, and FEI (currently Thermo Fisher Scientific).

FundersFunder number
GNS Science
Murdoch Charitable Trust
Tikitere Trust
National Science FoundationDEB-1134877
U.S. Department of EnergyDE-AC05-00OR22725
National Aeronautics and Space AdministrationNNX16AJ66G
M.J. Murdock Charitable Trust
Oak Ridge National Laboratory

    Keywords

    • Desulfurococcaceae
    • Nanoarchaeota
    • Terrestrial hot spring
    • Thermophile

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