Gallionellaceae pangenomic analysis reveals insight into phylogeny, metabolic flexibility, and iron oxidation mechanisms

Hoover, Rene L; Keffer, Jessica L.; Polson, Shawn W.; Chan, Clara S.

doi:10.1101/2023.01.26.525709

Cited by 5 publications

(13 citation statements)

References 133 publications

(235 reference statements)

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“…The rhizosphere genome bin 9BH_112 is closely related to the rice paddy soil isolate Ferrigenium kumadai An22, (90.1% ANI/91.5% AAI); however, GTDB classifies AN22 and bin 9BH_112 as Gallionella, which is also confirmed by our phylogenetic analysis based on 13 concatenated ribosomal protein sequences ( Fig. 6 ; details in methods and (35)). Thus, going forward, we refer to bin 9BH_112 as Gallionella 9BH_112 with the understanding that it is closely related to F. kumadai An22.…”

Section: Resultssupporting

confidence: 71%

“…S. lithotrophicus ES-1 similarly has sox and dsr genes, and is able to grow by thiosulfate oxidation. Based on previous phylogenetic analysis, the DsrAB from ES-1 and the four 9BB/9BH Gallionellaceae genomes cluster with reverse DSR (rDSR) (35).…”

Section: Resultsmentioning

confidence: 99%

“…Hydrogenase genes are common amongst FeOB (e.g. (35, 72, 73)) and other bacteria, and may play a role in providing reducing equivalents for carbon and nitrogen fixation since the Fe(II)/Fe(III) redox potential is relatively high and requires reverse electron transport to produce NADH and ferredoxin. The variety of hydrogenases implies a range of roles, which may also include growth on hydrogen as well as fermentation, with hydrogen formation serving as an electron sink (see below).…”

Section: Resultsmentioning

confidence: 99%

“…All four 9BB/9BH Gallionellaceae genomes have genes for microaerophilic iron oxidation. The genomes contain the iron oxidase gene cyc2, which is characteristic of most Gallionellaceae (35). They lack mtoAB, an outer membrane multiheme cytochrome-porin complex associated with iron oxidation in S. lithotrophicus ES-1 (68)(69)(70).…”

Section: Feob Energy Metabolisms -Electron Donors and Acceptorsmentioning

confidence: 99%

“…(24). While the isolate An22 was named Ferrigenium based on 16S rRNA gene dissimilarity from Gallionella, subsequent full-genome analyses showed that it is a Gallionella (35). Gallionellaceae have also been identified using 16S rRNA gene analyses including universal and taxa-specific primers in paddy soil and the rice rhizosphere (31,(36)(37)(38)(39).…”

Section: Introductionmentioning

confidence: 99%

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Gallionellaceae in rice root plaque: metabolic roles in iron oxidation, nutrient cycling, and plant interactions

Chan

Dykes

Hoover

et al. 2023

Preprint

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On the roots of wetland plants such as rice, iron oxidation forms iron-rich plaques that modulate plant nutrient and metal uptake. An enduring question is whether microbes catalyze this iron oxidation and, furthermore, if these iron-oxidizers mediate other important biogeochemical and plant interactions. To investigate this, we studied the microbial communities, metagenomes, and geochemistry of iron plaque on field-grown rice, as well as the surrounding rhizosphere and bulk soil. Plaque iron content (per mass root) increased over the growing season, showing continuous deposition. Analysis of 16S rRNA genes showed abundant iron-oxidizing and iron-reducing bacteria (FeOB and FeRB) in plaque, rhizosphere and bulk soil. FeOB were enriched in plaque, suggesting FeOB affinity for the root surface. Gallionellaceae FeOBSideroxydanswere enriched during the vegetative and early reproductive rice growth stages, while aGallionellawas enriched during reproduction through grain maturity, suggesting distinct FeOB niches over the rice life cycle. FeRBAnaeromyxobacterandGeobacterincreased in plaque later, during reproduction and grain ripening, corresponding to increased plaque iron. Metagenome-assembled genomes reveal that the Gallionellaceae may grow mixotrophically using both Fe(II) and organics. TheSideroxydansare facultative, able to use non-Fe substrates, which may allow colonization of rice roots early in the season. FeOB genomes suggest adaptations for interacting with plants, including colonization, immunity, utilization of plant organics, and nitrogen fixation. Together, our results strongly suggest that rhizoplane and rhizosphere FeOB are specifically associated with the rice plants, catalyzing the formation of iron plaque, with the potential to contribute to plant growth.

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Section: Resultssupporting

confidence: 71%

Section: Resultsmentioning

confidence: 99%

Section: Resultsmentioning

confidence: 99%

Section: Feob Energy Metabolisms -Electron Donors and Acceptorsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Gallionellaceae in rice root plaque: metabolic roles in iron oxidation, nutrient cycling, and plant interactions

Chan

Dykes

Hoover

et al. 2023

Preprint

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Ferriphaselus amnicola strain GF-20, a new iron- and thiosulfate-oxidizing bacterium isolated from a hard rock aquifer

Garry,

Farasin,

Drevillon

et al. 2024

FEMS Microbiology Ecology

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Ferriphaselus amnicola GF-20 is the first Fe-oxidizing bacterium isolated from the continental subsurface. It was isolated from groundwater circulating at 20 m depth in the fractured-rock catchment observatory of Guidel-Ploemeur (France). Strain GF-20 is a neutrophilic, iron- and thiosulfate-oxidizer and grows autotrophically. The strain shows a preference for low oxygen concentrations, which suggests an adaptation to the limiting oxygen conditions of the subsurface. It produces extracellular stalks and dreads when grown with Fe(II) but does not secrete any structure when grown with thiosulfate. Phylogenetic analyses and genome comparisons revealed that strain GF-20 is affiliated with the species Ferriphaselus amnicola and is strikingly similar to Ferriphaselus amnicola strain OYT1 which was isolated from a groundwater seep in Japan. Based on the phenotypic and phylogenetic characteristics, we propose that GF-20 represents a new strain within the species Ferriphaselus amnicola.

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Adaptation strategies of iron-oxidizing bacteriaGallionellaand Zetaproteobacteria crossing the marine–freshwater barrier

Hribovšek,

Denny,

Mall

et al. 2024

Preprint

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Iron-oxidizing Betaproteobacteria and Zetaproteobacteria are generally associated with freshwater and marine environments, respectively. Despite repeated cross-environment observations of these taxa, there has been no focused exploration of genomes of marineGallionella(Betaproteobacteria) to understand transitions between freshwater and marine habitats. Consequently, their roles in these environments remain uncertain. Here, we present strong evidence for co-occurrence ofGallionellaand Zetaproteobacteria at deep-sea hydrothermal vents at the Arctic Mid-Ocean Ridges through metagenomic analyses. Phylogenomics analysis ofGallionellametagenome-assembled genomes (MAGs) suggests that seawater adaptation is an evolutionary event which occurred multiple times in distinct lineages. Similarly, several distinct evolutionary events for freshwater and terrestrialMariprofundusand other Zetaproteobacteria are predicted. The presence ofcyc2iron oxidation genes in co-occurring marine Betaproteobacteria and Zetaproteobacteria implies an overlap in niches of these iron-oxidizers. Functional enrichment analyses reveal genetic differences between marine MAGs of both iron-oxidizing groups and their terrestrial aquatic counterparts linked to salinity adaptation. Though scanning electron microscopy confirms the presence of Fe(III) oxyhydroxide stalks whereGallionellaandMariprofundusco-occur,GallionellaMAGs from hydrothermal vents lack evidence of putative stalk formation genes.Mariprofundusis therefore the likely sole stalk-producing iron-oxidizer in this environment. Conversely, discovery of putative stalk formation genes inMariprofundusMAGs across the marine-freshwater barrier suggests that Fe(III) oxyhydroxide stalks might not be an exclusive signature for single iron-oxidizing taxa in marine and freshwater environments. Our research provides novel insights into the iron-oxidizing capacities, stalk production, environmental adaptation, and evolutionary transitions between marine and freshwater habitats forGallionellaand Zetaproteobacteria.

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Gallionellaceae pangenomic analysis reveals insight into phylogeny, metabolic flexibility, and iron oxidation mechanisms

Cited by 5 publications

References 133 publications

Gallionellaceae in rice root plaque: metabolic roles in iron oxidation, nutrient cycling, and plant interactions

Gallionellaceae in rice root plaque: metabolic roles in iron oxidation, nutrient cycling, and plant interactions

Ferriphaselus amnicola strain GF-20, a new iron- and thiosulfate-oxidizing bacterium isolated from a hard rock aquifer

Adaptation strategies of iron-oxidizing bacteriaGallionellaand Zetaproteobacteria crossing the marine–freshwater barrier

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