Comparative genomic insights into ecophysiology of neutrophilic, microaerophilic iron oxidizing bacteria

Shingo Kato, Moriya Ohkuma, Deborah H. Powell, Sean T. Krepski, Kenshiro Oshima, Masahira Hattori, Nicole Shapiro, Tanja Woyke, Clara S. Chan

Research output: Contribution to journalArticle

26 Citations (Scopus)

Abstract

Neutrophilic microaerophilic iron-oxidizing bacteria (FeOB) are thought to play a significant role in cycling of carbon, iron and associated elements in both freshwater and marine iron-rich environments. However, the roles of the neutrophilic microaerophilic FeOB are still poorly understood due largely to the difficulty of cultivation and lack of functional gene markers. Here, we analyze the genomes of two freshwater neutrophilic microaerophilic stalk-forming FeOB, Ferriphaselus amnicola OYT1 and Ferriphaselus strain R-1. Phylogenetic analyses confirm that these are distinct species within Betaproteobacteria; we describe strain R-1 and propose the name F. globulitus. We compare the genomes to those of two freshwater Betaproteobacterial and three marine Zetaproteobacterial FeOB isolates in order to look for mechanisms common to all FeOB, or just stalk-forming FeOB. The OYT1 and R-1 genomes both contain homologs to cyc2, which encodes a protein that has been shown to oxidize Fe in the acidophilic FeOB, Acidithiobacillus ferrooxidans. This c-type cytochrome common to all seven microaerophilic FeOB isolates, strengthening the case for its common utility in the Fe oxidation pathway. In contrast, the OYT1 and R-1 genomes lack mto genes found in other freshwater FeOB. OYT1 and R-1 both have genes that suggest they can oxidize sulfur species. Both have the genes necessary to fix carbon by the Calvin-Benson-Basshom pathway, while only OYT1 has the genes necessary to fix nitrogen. The stalk-forming FeOB share xag genes that may help form the polysaccharide structure of stalks. Both OYT1 and R-1 make a novel biomineralization structure, short rod-shaped Fe oxyhydroxides much smaller than their stalks; these oxides are constantly shed, and may be a vector for C, P, and metal transport to downstream environments. Our results show that while different FeOB are adapted to particular niches, freshwater and marine FeOB likely share common mechanisms for Fe oxidation electron transport and biomineralization pathways.

Original languageEnglish
Article number1265
JournalFrontiers in Microbiology
Volume6
Issue numberNOV
DOIs
Publication statusPublished - 2015
Externally publishedYes

Fingerprint

Fresh Water
Iron
Bacteria
Genome
Genes
Carbon
Acidithiobacillus
Cytochrome c Group
Betaproteobacteria
Electron Transport
Sulfur
Oxides
Names
Polysaccharides
Nitrogen
Metals
Proteins

Keywords

  • Biomineralization
  • Ferriphaselus
  • Gallionellales
  • Iron oxidation
  • Iron-oxidizing bacteria

ASJC Scopus subject areas

  • Microbiology
  • Microbiology (medical)

Cite this

Comparative genomic insights into ecophysiology of neutrophilic, microaerophilic iron oxidizing bacteria. / Kato, Shingo; Ohkuma, Moriya; Powell, Deborah H.; Krepski, Sean T.; Oshima, Kenshiro; Hattori, Masahira; Shapiro, Nicole; Woyke, Tanja; Chan, Clara S.

In: Frontiers in Microbiology, Vol. 6, No. NOV, 1265, 2015.

Research output: Contribution to journalArticle

Kato, S, Ohkuma, M, Powell, DH, Krepski, ST, Oshima, K, Hattori, M, Shapiro, N, Woyke, T & Chan, CS 2015, 'Comparative genomic insights into ecophysiology of neutrophilic, microaerophilic iron oxidizing bacteria', Frontiers in Microbiology, vol. 6, no. NOV, 1265. https://doi.org/10.3389/fmicb.2015.01265
Kato, Shingo ; Ohkuma, Moriya ; Powell, Deborah H. ; Krepski, Sean T. ; Oshima, Kenshiro ; Hattori, Masahira ; Shapiro, Nicole ; Woyke, Tanja ; Chan, Clara S. / Comparative genomic insights into ecophysiology of neutrophilic, microaerophilic iron oxidizing bacteria. In: Frontiers in Microbiology. 2015 ; Vol. 6, No. NOV.
@article{bc471816da5d4d908d2bbba5871bebaf,
title = "Comparative genomic insights into ecophysiology of neutrophilic, microaerophilic iron oxidizing bacteria",
abstract = "Neutrophilic microaerophilic iron-oxidizing bacteria (FeOB) are thought to play a significant role in cycling of carbon, iron and associated elements in both freshwater and marine iron-rich environments. However, the roles of the neutrophilic microaerophilic FeOB are still poorly understood due largely to the difficulty of cultivation and lack of functional gene markers. Here, we analyze the genomes of two freshwater neutrophilic microaerophilic stalk-forming FeOB, Ferriphaselus amnicola OYT1 and Ferriphaselus strain R-1. Phylogenetic analyses confirm that these are distinct species within Betaproteobacteria; we describe strain R-1 and propose the name F. globulitus. We compare the genomes to those of two freshwater Betaproteobacterial and three marine Zetaproteobacterial FeOB isolates in order to look for mechanisms common to all FeOB, or just stalk-forming FeOB. The OYT1 and R-1 genomes both contain homologs to cyc2, which encodes a protein that has been shown to oxidize Fe in the acidophilic FeOB, Acidithiobacillus ferrooxidans. This c-type cytochrome common to all seven microaerophilic FeOB isolates, strengthening the case for its common utility in the Fe oxidation pathway. In contrast, the OYT1 and R-1 genomes lack mto genes found in other freshwater FeOB. OYT1 and R-1 both have genes that suggest they can oxidize sulfur species. Both have the genes necessary to fix carbon by the Calvin-Benson-Basshom pathway, while only OYT1 has the genes necessary to fix nitrogen. The stalk-forming FeOB share xag genes that may help form the polysaccharide structure of stalks. Both OYT1 and R-1 make a novel biomineralization structure, short rod-shaped Fe oxyhydroxides much smaller than their stalks; these oxides are constantly shed, and may be a vector for C, P, and metal transport to downstream environments. Our results show that while different FeOB are adapted to particular niches, freshwater and marine FeOB likely share common mechanisms for Fe oxidation electron transport and biomineralization pathways.",
keywords = "Biomineralization, Ferriphaselus, Gallionellales, Iron oxidation, Iron-oxidizing bacteria",
author = "Shingo Kato and Moriya Ohkuma and Powell, {Deborah H.} and Krepski, {Sean T.} and Kenshiro Oshima and Masahira Hattori and Nicole Shapiro and Tanja Woyke and Chan, {Clara S.}",
year = "2015",
doi = "10.3389/fmicb.2015.01265",
language = "English",
volume = "6",
journal = "Frontiers in Microbiology",
issn = "1664-302X",
publisher = "Frontiers Media S. A.",
number = "NOV",

}

TY - JOUR

T1 - Comparative genomic insights into ecophysiology of neutrophilic, microaerophilic iron oxidizing bacteria

AU - Kato, Shingo

AU - Ohkuma, Moriya

AU - Powell, Deborah H.

AU - Krepski, Sean T.

AU - Oshima, Kenshiro

AU - Hattori, Masahira

AU - Shapiro, Nicole

AU - Woyke, Tanja

AU - Chan, Clara S.

PY - 2015

Y1 - 2015

N2 - Neutrophilic microaerophilic iron-oxidizing bacteria (FeOB) are thought to play a significant role in cycling of carbon, iron and associated elements in both freshwater and marine iron-rich environments. However, the roles of the neutrophilic microaerophilic FeOB are still poorly understood due largely to the difficulty of cultivation and lack of functional gene markers. Here, we analyze the genomes of two freshwater neutrophilic microaerophilic stalk-forming FeOB, Ferriphaselus amnicola OYT1 and Ferriphaselus strain R-1. Phylogenetic analyses confirm that these are distinct species within Betaproteobacteria; we describe strain R-1 and propose the name F. globulitus. We compare the genomes to those of two freshwater Betaproteobacterial and three marine Zetaproteobacterial FeOB isolates in order to look for mechanisms common to all FeOB, or just stalk-forming FeOB. The OYT1 and R-1 genomes both contain homologs to cyc2, which encodes a protein that has been shown to oxidize Fe in the acidophilic FeOB, Acidithiobacillus ferrooxidans. This c-type cytochrome common to all seven microaerophilic FeOB isolates, strengthening the case for its common utility in the Fe oxidation pathway. In contrast, the OYT1 and R-1 genomes lack mto genes found in other freshwater FeOB. OYT1 and R-1 both have genes that suggest they can oxidize sulfur species. Both have the genes necessary to fix carbon by the Calvin-Benson-Basshom pathway, while only OYT1 has the genes necessary to fix nitrogen. The stalk-forming FeOB share xag genes that may help form the polysaccharide structure of stalks. Both OYT1 and R-1 make a novel biomineralization structure, short rod-shaped Fe oxyhydroxides much smaller than their stalks; these oxides are constantly shed, and may be a vector for C, P, and metal transport to downstream environments. Our results show that while different FeOB are adapted to particular niches, freshwater and marine FeOB likely share common mechanisms for Fe oxidation electron transport and biomineralization pathways.

AB - Neutrophilic microaerophilic iron-oxidizing bacteria (FeOB) are thought to play a significant role in cycling of carbon, iron and associated elements in both freshwater and marine iron-rich environments. However, the roles of the neutrophilic microaerophilic FeOB are still poorly understood due largely to the difficulty of cultivation and lack of functional gene markers. Here, we analyze the genomes of two freshwater neutrophilic microaerophilic stalk-forming FeOB, Ferriphaselus amnicola OYT1 and Ferriphaselus strain R-1. Phylogenetic analyses confirm that these are distinct species within Betaproteobacteria; we describe strain R-1 and propose the name F. globulitus. We compare the genomes to those of two freshwater Betaproteobacterial and three marine Zetaproteobacterial FeOB isolates in order to look for mechanisms common to all FeOB, or just stalk-forming FeOB. The OYT1 and R-1 genomes both contain homologs to cyc2, which encodes a protein that has been shown to oxidize Fe in the acidophilic FeOB, Acidithiobacillus ferrooxidans. This c-type cytochrome common to all seven microaerophilic FeOB isolates, strengthening the case for its common utility in the Fe oxidation pathway. In contrast, the OYT1 and R-1 genomes lack mto genes found in other freshwater FeOB. OYT1 and R-1 both have genes that suggest they can oxidize sulfur species. Both have the genes necessary to fix carbon by the Calvin-Benson-Basshom pathway, while only OYT1 has the genes necessary to fix nitrogen. The stalk-forming FeOB share xag genes that may help form the polysaccharide structure of stalks. Both OYT1 and R-1 make a novel biomineralization structure, short rod-shaped Fe oxyhydroxides much smaller than their stalks; these oxides are constantly shed, and may be a vector for C, P, and metal transport to downstream environments. Our results show that while different FeOB are adapted to particular niches, freshwater and marine FeOB likely share common mechanisms for Fe oxidation electron transport and biomineralization pathways.

KW - Biomineralization

KW - Ferriphaselus

KW - Gallionellales

KW - Iron oxidation

KW - Iron-oxidizing bacteria

UR - http://www.scopus.com/inward/record.url?scp=84949779399&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84949779399&partnerID=8YFLogxK

U2 - 10.3389/fmicb.2015.01265

DO - 10.3389/fmicb.2015.01265

M3 - Article

VL - 6

JO - Frontiers in Microbiology

JF - Frontiers in Microbiology

SN - 1664-302X

IS - NOV

M1 - 1265

ER -