Diversification and niche adaptations of Nitrospina-like bacteria in the polyextreme interfaces of Red Sea brines

Handle URI:
http://hdl.handle.net/10754/592505
Title:
Diversification and niche adaptations of Nitrospina-like bacteria in the polyextreme interfaces of Red Sea brines
Authors:
Ngugi, David ( 0000-0002-0442-4279 ) ; Blom, Jochen; Stepanauskas, Ramunas ( 0000-0003-4458-3108 ) ; Stingl, Ulrich ( 0000-0002-0684-2597 )
Abstract:
Nitrite-oxidizing bacteria (NOB) of the genus Nitrospina have exclusively been found in marine environments. In the brine–seawater interface layer of Atlantis II Deep (Red Sea), Nitrospina-like bacteria constitute up to one-third of the bacterial 16S ribosomal RNA (rRNA) gene sequences. This is much higher compared with that reported in other marine habitats (~10% of all bacteria), and was unexpected because no NOB culture has been observed to grow above 4.0% salinity, presumably due to the low net energy gained from their metabolism that is insufficient for both growth and osmoregulation. Using phylogenetics, single-cell genomics and metagenomic fragment recruitment approaches, we document here that these Nitrospina-like bacteria, designated as Candidatus Nitromaritima RS, are not only highly diverged from the type species Nitrospina gracilis (pairwise genome identity of 69%) but are also ubiquitous in the deeper, highly saline interface layers (up to 11.2% salinity) with temperatures of up to 52 °C. Comparative pan-genome analyses revealed that less than half of the predicted proteome of Ca. Nitromaritima RS is shared with N. gracilis. Interestingly, the capacity for nitrite oxidation is also conserved in both genomes. Although both lack acidic proteomes synonymous with extreme halophiles, the pangenome of Ca. Nitromaritima RS specifically encodes enzymes with osmoregulatory and thermoprotective roles (i.e., ectoine/hydroxyectoine biosynthesis) and of thermodynamic importance (i.e., nitrate and nitrite reductases). Ca. Nitromaritima RS also possesses many hallmark traits of microaerophiles and high-affinity NOB. The abundance of the uncultured Ca. Nitromaritima lineage in marine oxyclines suggests their unrecognized ecological significance in deoxygenated areas of the global ocean.
KAUST Department:
Red Sea Research Center (RSRC)
Citation:
Diversification and niche adaptations of Nitrospina-like bacteria in the polyextreme interfaces of Red Sea brines 2015 The ISME Journal
Publisher:
Springer Nature
Journal:
The ISME Journal
Issue Date:
11-Dec-2015
DOI:
10.1038/ismej.2015.214
Type:
Article
ISSN:
1751-7362; 1751-7370
Additional Links:
http://www.nature.com/doifinder/10.1038/ismej.2015.214
Appears in Collections:
Articles; Red Sea Research Center (RSRC)

Full metadata record

DC FieldValue Language
dc.contributor.authorNgugi, Daviden
dc.contributor.authorBlom, Jochenen
dc.contributor.authorStepanauskas, Ramunasen
dc.contributor.authorStingl, Ulrichen
dc.date.accessioned2015-12-22T06:23:04Zen
dc.date.available2015-12-22T06:23:04Zen
dc.date.issued2015-12-11en
dc.identifier.citationDiversification and niche adaptations of Nitrospina-like bacteria in the polyextreme interfaces of Red Sea brines 2015 The ISME Journalen
dc.identifier.issn1751-7362en
dc.identifier.issn1751-7370en
dc.identifier.doi10.1038/ismej.2015.214en
dc.identifier.urihttp://hdl.handle.net/10754/592505en
dc.description.abstractNitrite-oxidizing bacteria (NOB) of the genus Nitrospina have exclusively been found in marine environments. In the brine–seawater interface layer of Atlantis II Deep (Red Sea), Nitrospina-like bacteria constitute up to one-third of the bacterial 16S ribosomal RNA (rRNA) gene sequences. This is much higher compared with that reported in other marine habitats (~10% of all bacteria), and was unexpected because no NOB culture has been observed to grow above 4.0% salinity, presumably due to the low net energy gained from their metabolism that is insufficient for both growth and osmoregulation. Using phylogenetics, single-cell genomics and metagenomic fragment recruitment approaches, we document here that these Nitrospina-like bacteria, designated as Candidatus Nitromaritima RS, are not only highly diverged from the type species Nitrospina gracilis (pairwise genome identity of 69%) but are also ubiquitous in the deeper, highly saline interface layers (up to 11.2% salinity) with temperatures of up to 52 °C. Comparative pan-genome analyses revealed that less than half of the predicted proteome of Ca. Nitromaritima RS is shared with N. gracilis. Interestingly, the capacity for nitrite oxidation is also conserved in both genomes. Although both lack acidic proteomes synonymous with extreme halophiles, the pangenome of Ca. Nitromaritima RS specifically encodes enzymes with osmoregulatory and thermoprotective roles (i.e., ectoine/hydroxyectoine biosynthesis) and of thermodynamic importance (i.e., nitrate and nitrite reductases). Ca. Nitromaritima RS also possesses many hallmark traits of microaerophiles and high-affinity NOB. The abundance of the uncultured Ca. Nitromaritima lineage in marine oxyclines suggests their unrecognized ecological significance in deoxygenated areas of the global ocean.en
dc.language.isoenen
dc.publisherSpringer Natureen
dc.relation.urlhttp://www.nature.com/doifinder/10.1038/ismej.2015.214en
dc.rightsThis work is licensed under a Creative Commons Attribution-NonCommercial-ShareAlike 4.0 International License. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in the credit line; if the material is not included under the Creative Commons license, users will need to obtain permission from the license holder to reproduce the material. To view a copy of this license, visit http://creativecommons.org/licenses/by-nc-sa/4.0/.en
dc.titleDiversification and niche adaptations of Nitrospina-like bacteria in the polyextreme interfaces of Red Sea brinesen
dc.typeArticleen
dc.contributor.departmentRed Sea Research Center (RSRC)en
dc.identifier.journalThe ISME Journalen
dc.eprint.versionPublisher's Version/PDFen
dc.contributor.institutionBioinformatics and Systems Biology, Justus Liebig University Giessen, Germanyen
dc.contributor.institutionBigelow Laboratories for Ocean Sciences, East Boothbay, ME 04544-0380, USAen
dc.contributor.affiliationKing Abdullah University of Science and Technology (KAUST)en
kaust.authorNgugi, Daviden
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