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

Chan, Clara S.; Dykes, Gretchen E.; Hoover, Rene L.; Limmer, Matt A.; Seyfferth, Angelia L.

doi:10.1128/aem.00570-23

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

Journal Article · Mon Nov 27 00:00:00 EST 2023 · Applied and Environmental Microbiology

DOI:https://doi.org/10.1128/aem.00570-23· OSTI ID:2471682

^[1]; Dykes, Gretchen E. ^[2]; ^[1]; Limmer, Matt A. ^[3]; ^[3]

Univ. of Delaware, Newark, DE (United States); Delaware Biotechnology Institute, Newark, DE (United States)
Univ. of Delaware, Newark, DE (United States); Delaware Biotechnology Institute, Newark, DE (United States); US Environmental Protection Agency (EPA), Washington, DC (United States)
Univ. of Delaware, Newark, DE (United States)

On the roots of wetland plants such as rice, Fe(II) oxidation forms Fe(III) oxyhydroxide-rich plaques that modulate plant nutrient and metal uptake. The microbial roles in catalyzing this oxidation have been debated and it is unclear 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, plus 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 Fe(II)-oxidizing and Fe(III)-reducing bacteria (FeOB and FeRB) in plaque, rhizosphere, and bulk soil. FeOB were enriched in relative abundance in plaque, suggesting FeOB affinity for the root surface. Gallionellaceae FeOB Sideroxydans were enriched during vegetative and early reproductive rice growth stages, while a Gallionella was enriched during reproduction through grain maturity, suggesting distinct FeOB niches over the rice life cycle. FeRB Anaeromyxobacter and Geobacter increased in plaque later, during reproduction and grain ripening, corresponding to increased plaque iron. Metagenome-assembled genomes revealed that Gallionellaceae may grow mixotrophically using both Fe(II) and organics. The Sideroxydans are 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, plant immunity defense, utilization of plant organics, and nitrogen fixation. Taken together, our results strongly suggest that rhizoplane and rhizosphere FeOB can specifically associate with rice roots, catalyzing iron plaque formation, with the potential to contribute to plant growth.

View Accepted Manuscript (DOE)

Research Organization:: SLAC National Accelerator Laboratory (SLAC), Menlo Park, CA (United States). Stanford Synchrotron Radiation Lightsource (SSRL)

Sponsoring Organization:: National Science Foundation (NSF); USDA; USDOE Office of Science (SC), Basic Energy Sciences (BES)

Grant/Contract Number:: AC02-76SF00515

OSTI ID:: 2471682

Journal Information:: Applied and Environmental Microbiology, Journal Name: Applied and Environmental Microbiology Journal Issue: 12 Vol. 89; ISSN 0099-2240

Publisher:: American Society for MicrobiologyCopyright Statement

Country of Publication:: United States

Language:: English

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