Novel Pelagic Iron-Oxidizing Zetaproteobacteria from the Chesapeake Bay Oxic–Anoxic Transition Zone

Abstract

Chemolithotrophic iron-oxidizing bacteria (FeOB) could theoretically inhabit any environment where Fe(II) and O2 (or nitrate) coexist. Until recently, marine Fe-oxidizing Zetaproteobacteria had primarily been observed in benthic and subsurface settings, but not redox-stratified water columns. This may be due to the challenges that a pelagic lifestyle would pose for Zetaproteobacteria, given low Fe(II) concentrations in modern marine waters and the possibility that Fe oxyhydroxide biominerals could cause cells to sink. However, we recently cultivated Zetaproteobacteria from the Chesapeake Bay oxic–anoxic transition zone, suggesting that they can survive and contribute to biogeochemical cycling in a stratified estuary. Here we describe the isolation, characterization, and genomes of two new species, Mariprofundus aestuarium CP-5 and Mariprofundus ferrinatatus CP-8, which are the first Zetaproteobacteria isolates from a pelagic environment. We looked for adaptations enabling strains CP-5 and CP-8 to overcome the challenges of living in a low Fe redoxcline with frequent O2 fluctuations due to tidal mixing. We found that the CP strains produce distinctive dreadlock-like Fe oxyhydroxide structures that are easily shed, which would help cells maintain suspension in the water column. These oxides are by-products of Fe(II) oxidation, likely catalyzed by the putative Fe(II) oxidase encoded by the cyc2 gene, present in both CP-5 and CP-8 genomes; the consistent presence of cyc2 in all microaerophilic FeOB and other FeOB genomes supports its putative role in Fe(II) oxidation. The CP strains also have two gene clusters associated with biofilm formation (Wsp system and the Widespread Colonization Island) that are absent or rare in other Zetaproteobacteria. We propose that biofilm formation enables the CP strains to attach to FeS particles and form flocs, an advantageous strategy for scavenging Fe(II) and developing low [O2] microenvironments within more oxygenated waters. However, the CP strains appear to be adapted to somewhat higher concentrations of O2, as indicated by the presence of genes encoding aa3-type cytochrome c oxidases, but not the cbb3-type found in all other Zetaproteobacteria isolate genomes. Overall, our results reveal adaptations for life in a physically dynamic, low Fe(II) water column, suggesting that niche-specific strategies can enable Zetaproteobacteria to live in any environment with Fe(II).

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

“…The distribution of Fe revealed by BSE‐SEM (Figure c–h) demonstrates that these textural features are composed of silicified twisted stalks. While some Fe‐oxidizing species are known to form dendrite‐like extracellular structures (Chiu, Kato, McAllister, Field, & Chan, ; Edwards, Rogers, Wirsen, & McCollom, ), dendritic growth of stalks produced by Mariprofundus ferrooxydans or other benthic Zetaproteobacteria has not previously been reported. Twisted stalks have been discovered in association with Frutexites ‐like iron shrubs in biofilms with active Fe and N‐cycling, but were not found to constitute the main framework of these dendrites (Heim, Quéric, Ionescu, Schäfer, & Reitner, ).…”

The distribution of active iron‐cycling bacteria in marine and freshwater sediments is decoupled from geochemical gradients

“…Microorganisms that oxidize Fe(II) and reduce Fe(III) have been reported from various Fe‐rich environments (>1 wt % Fe) such as hot springs (Kasama and Murakami, ), ferrous hydrothermal vents (Emerson and Moyer, ; Edwards et al ., ; Fitzsimmons et al ., ), Fe seeps and springs (Blöthe and Roden, ; Hegler et al ., ), rice paddy soils (Li et al ., ; Peng et al ., ), salt lake sediment (Emmerich et al ., ), microbial mats in the arctic tundra and in close proximity of hydrothermal vents (Emerson et al ., ) and ponds (Bruun et al ., ). In contrast, iron‐poor environments (with relatively low, i.e., micromolar, concentrations of Fe(II)) remained relatively unexplored, however, very recently, microbial Fe‐cycling has also been described for environments with low Fe content (Laufer et al ., ; Chiu et al ., ).…”

Marine Fe-oxidizingZetaproteobacteria: Historical, ecological, and genomic perspectives

“…With this experiment, we have shown that PV-1 outpaces abiotic oxidation below 49 μM O 2 , and accounts for up to 99% of the Fe oxidation at 10 μM O 2 (Figure 1; Table 3). In cultures of M. aestuarium CP-5 and M. ferrinatatus CP-8, oxygen concentrations ranged from 0.07-2.0 μM O 2 within the cell growth band (25). This range of O 2 growth conditions is well below the level at which almost all Fe oxidation was biotic for PV-1, suggesting that many Zetaproteobacteria are well adapted to compete and thrive under micromolar and submicromolar O 2 concentrations.…”

“…While most Zetaproteobacteria isolates form a stalk, some make other biomineral morphologies (Table 1; Figure 3A). Mariprofundus ferrinatatus CP-8 and M. aestuarium CP-5 form shorter filaments that resemble the dreadlock hairstyle (Figure 3C) (25). Dreads were originally observed in terrestrial FeOB Gallionellaceae Ferriphaselus spp.…”

“…Fe(II) can also come from natural sources in coastal environments, originating from mineral weathering and transported in anoxic groundwater. Fe redox cycling at the oxic-anoxic transition zone of stratified estuaries can support the growth of Zetaproteobacteria , as evidenced by the isolation of M. ferrinatatus CP-8 and M. aestuarium CP-5 (25, 26). In near shore sediments, Fe-rich groundwater can support microbial communities with Zetaproteobacteria at the sediment surface (69–71).…”