The Fe(II)-oxidizingZetaproteobacteria: historical, ecological and genomic perspectives

Abstract

The Zetaproteobacteria are a class of bacteria typically associated with marine Fe(II)-oxidizing environments. First discovered in the hydrothermal vents at Loihi Seamount, Hawaii, they have become model organisms for marine microbial Fe(II) oxidation. In addition to deep sea and shallow hydrothermal vents, Zetaproteobacteria are found in coastal sediments, other marine subsurface environments, steel corrosion biofilms and saline terrestrial springs. Isolates from a range of environments all grow by autotrophic Fe(II) oxidation. Their success lies partly in their microaerophily, which enables them to compete with abiotic Fe(II) oxidation at Fe(II)-rich oxic/anoxic transition zones. To determine the known diversity of the Zetaproteobacteria , we have used 16S rRNA gene sequences to define 59 operational taxonomic units (OTUs), at 97% similarity. While some Zetaproteobacteria taxa appear to be cosmopolitan, others are enriched by specific habitats. OTU networks show that certain Zetaproteobacteria co-exist, sharing compatible niches. These niches may correspond with adaptations to O 2 , H 2 and nitrate availability, based on genomic analyses of metabolic potential. Also, a putative Fe(II) oxidation gene has been found in diverse Zetaproteobacteria taxa, suggesting that the Zetaproteobacteria evolved as Fe(II) oxidation specialists. In all, studies suggest that Zetaproteobacteria are widespread, and therefore may have a broad influence on marine and saline terrestrial Fe cycling.

Validating the Cyc2 Neutrophilic Iron Oxidation Pathway Using Meta-omics of Zetaproteobacteria Iron Mats at Marine Hydrothermal Vents

“…Mariana mats had shallow O 2 gradients, while at Loihi, O 2 was undetectable (Ͻ3 M) at 1 cm below the mat surface. These Fe(II) and O 2 conditions favor biotic Fe oxidation (10). At Mariana, total dissolved Fe was depleted by 49% to 74% in our low-temperature mats relative to the conservative mixing of the local high-temperature zero-Mg endmember (Fig.…”

“…Comparative genomics has led to multiple proposed pathways, each involving an outer membrane cytochrome (5)(6)(7). However, only one pathway is present in all well-established neutrophilic Fe-oxidizing isolates (Zetaproteobacteria and Gallionellaceae), centering on a fused cytochrome-porin, Cyc2 (7)(8)(9)(10). Yet, beyond comparative genomics, we lack evidence of the Cyc2 pathway function in neutrophilic Fe oxidizers, particularly the uncultured Fe oxidizers that dominate natural Fe systems.…”

“…To this end, we turned to Zetaproteobacteria in natural Fe microbial mats. The Zetaproteobacteria discovered to date are all considered to be Fe oxidizers, since every isolate grows by Fe oxidation and uncultured Zetaproteobacteria are typically found in Fe-oxidizing environments (10,(16)(17)(18)(19)(20)(21). The Zetaproteobacteria are often the dominant organisms in marine hydrothermal Fe mats (22)(23)(24)(25), where they play a key role in mat formation (26).…”

Distribution and Succession of Microbial Communities Along the Dispersal Pathway of Hydrothermal Plumes on the Southwest Indian Ridge

“…Members of the Desulfurobacteriaceae (Aquificae) were found within both samples but at minor abundances (<1%). ζ-proteobacteria, that include well-known neutrophilic iron-oxidizers from hydrothermal vent areas (McAllister et al, 2019), were commonly detected from most rising buoyant plume and near-bottom seawater samples, with highest relative abundances in RRP_89 and RRP_90 of ∼2%, but less than 1% in other samples (Figures 4, 5 and Supplementary Table S3). Interestingly, other putative neutrophilic iron-oxidizing bacteria, belonging to the β-Proteobacteria family Gallionellaceae, were also exclusively found in the RRP_89 sample (Supplementary Table S3).…”

On the biogenicity of Fe‐oxyhydroxide filaments in silicified low‐temperature hydrothermal deposits: Implications for the identification of Fe‐oxidizing bacteria in the rock record

“…Fe‐oxyhydroxide deposits in modern low‐temperature hydrothermal environments on the seafloor commonly host Fe‐oxidizing Zetaproteobacteria (e.g., Emerson & Moyer, ; Forget, Murdock, & Juniper, ; Kato, Kobayashi, Kakegawa, & Yamagishi, ; Li et al, ; McAllister et al, ; Scott, Breier, Luther, & Emerson, ), which actively contribute to the growth of the deposits through biomineralization and stalk formation (e.g., Alt, ; Boyd & Scott, ; Edwards et al, ; Juniper & Fouquet, ; Karl, Brittain, & Tilbrook, ; Kennedy, Scott, & Ferris, ; Langley et al, ). These deposits may be similar to the sedimentary precursors of jaspers and iron formations, both with respect to mineralogy and genesis.…”