title: Metagenomic Analyses of the Autotrophic Fe(II)-Oxidizing, Nitrate-Reducing Enrichment Culture KS.
abstract: Nitrate-dependent ferrous iron [Fe(II)] oxidation (NDFO) is a well-recognized chemolithotrophic pathway in anoxic sediments. The neutrophilic chemolithoautotrophic enrichment culture KS originally obtained from a freshwater sediment (K. L. Straub, M. Benz, B. Schink, and F. Widdel, Appl Environ Microbiol 62:1458-1460, 1996) has been used as a model system to study NDFO. However, the primary Fe(II) oxidizer in this culture has not been isolated, despite extensive efforts to do so. Here, we present a metagenomic analysis of this enrichment culture in order to gain insight into electron transfer pathways and the roles of different bacteria in the culture. We obtained a near-complete genome of the primary Fe(II) oxidizer, a species in the family Gallionellaceae, and draft genomes from its flanking community members. A search of the putative extracellular electron transfer pathways in these genomes led to the identification of a homolog of the MtoAB complex [a porin-multiheme cytochromec system identified in neutrophilic microaerobic Fe(II)-oxidizing Sideroxydans lithotrophicus ES-1] in a Gallionellaceae sp., and findings of other putative genes involving cytochromecand multicopper oxidases, such as Cyc2 and OmpB. Genome-enabled metabolic reconstruction revealed that this Gallionellaceae sp. lacks nitric oxide and nitrous oxide reductase genes and may partner with flanking populations capable of complete denitrification to avoid toxic metabolite accumulation, which may explain its resistance to growth in pure culture. This and other revealed interspecies interactions and metabolic interdependencies in nitrogen and carbon metabolisms may allow these organisms to cooperate effectively to achieve robust chemolithoautotrophic NDFO. Overall, the results significantly expand our knowledge of NDFO and suggest a range of genetic targets for further exploration.
authors.affiliation: Department of Geoscience, University of Wisconsin-Madison, Madison, Wisconsin, USA she@wisc.edu eroden@geology.wisc.edu.|Department of Bacteriology, University of Wisconsin-Madison, Madison, Wisconsin, USA.|NASA Astrobiology Institute, University of Wisconsin-Madison, Madison, Wisconsin, USA.
authors.forename: Shaomei
authors.initials: S
authors.lastname: He
authors.affiliation: Geomicrobiology, Center for Applied Geosciences (ZAG), Eberhard Karls University Tuebingen, Tuebingen, Germany.
authors.forename: Claudia
authors.initials: C
authors.lastname: Tominski
authors.affiliation: Geomicrobiology, Center for Applied Geosciences (ZAG), Eberhard Karls University Tuebingen, Tuebingen, Germany.
authors.forename: Andreas
authors.initials: A
authors.lastname: Kappler
authors.affiliation: Department of Civil, Environmental, and Geo-Engineering, University of Minnesota, Minneapolis, Minnesota, USA.|BioTechnology Institute, University of Minnesota, St. Paul, Minnesota, USA.
authors.forename: Sebastian
authors.initials: S
authors.lastname: Behrens
authors.affiliation: Department of Geoscience, University of Wisconsin-Madison, Madison, Wisconsin, USA she@wisc.edu eroden@geology.wisc.edu.|NASA Astrobiology Institute, University of Wisconsin-Madison, Madison, Wisconsin, USA.
authors.forename: Eric E
authors.initials: EE
authors.lastname: Roden
mesh_terms: D052818:Autotrophic Processes; D003198:Computer Simulation; D003470:Culture Media; D004269:DNA, Bacterial / Q000235:genetics; D004579:Electron Transport; D005296:Ferrous Compounds / Q000378:metabolism*; D005618:Fresh Water; D043372:Gallionellaceae / Q000201:enzymology / Q000235:genetics* / Q000378:metabolism*; D019015:Geologic Sediments / Q000737:chemistry; D006859:Hydrogen / Q000378:metabolism; D053858:Metabolic Networks and Pathways; D056186:Metagenomics / Q000379:methods; D009566:Nitrates / Q000378:metabolism*; D010084:Oxidation-Reduction; D010088:Oxidoreductases / Q000235:genetics / Q000378:metabolism; D010802:Phylogeny; D012336:RNA, Ribosomal, 16S / Q000235:genetics; D017421:Sequence Analysis; D017422:Sequence Analysis, DNA
chemical_list: D003470:Culture Media; D004269:DNA, Bacterial; D005296:Ferrous Compounds; D009566:Nitrates; D012336:RNA, Ribosomal, 16S; D006859:Hydrogen; D010088:Oxidoreductases; C022763:nitrous oxide reductase