Biodiversity and Emerging Biogeography of the Neutrophilic Iron-Oxidizing Zetaproteobacteria

Abstract

Members of the neutrophilic iron-oxidizing candidate class Zetaproteobacteria have predominantly been found at sites of microbially mediated iron oxidation in marine environments around the Pacific Ocean. Eighty-four full-length (>1,400-bp) and 48 partial-length Zetaproteobacteria small-subunit (SSU) rRNA gene sequences from five novel clone libraries, one novel Zetaproteobacteria isolate, and the GenBank database were analyzed to assess the biodiversity of this burgeoning class of the Proteobacteria and to investigate its biogeography between three major sampling regions in the Pacific Ocean: Loihi Seamount, the Southern Mariana Trough, and the Tonga Arc. Sequences were grouped into operational taxonomic units (OTUs) on the basis of a 97% minimum similarity. Of the 28 OTUs detected, 13 were found to be endemic to one of the three main sampling regions and 2 were ubiquitous throughout the Pacific Ocean. Additionally, two deeply rooted OTUs that potentially dominate communities of iron oxidizers originating in the deep subsurface were identified. Spatial autocorrelation analysis and analysis of molecular variance (AMOVA) showed that geographic distance played a significant role in the distribution of Zetaproteobacteria biodiversity, whereas environmental parameters, such as temperature, pH, or total Fe concentration, did not have a significant effect. These results, detected using the coarse resolution of the SSU rRNA gene, indicate that the Zetaproteobacteria have a strong biogeographic signal.

Coexistence of Microaerophilic, Nitrate-Reducing, and Phototrophic Fe(II) Oxidizers and Fe(III) Reducers in Coastal Marine Sediment

“…M34, which was isolated as a microaerophilic Fe(II) oxidizer from a microbial mat at a deep-sea hydrothermal vent at Loihi Seamount (Hawaii) by McAllister et al (76). Our study thus shows that microaerophilic Fe(II)-oxidizing Zetaproteobacteria are also naturally present in coastal marine sediments.…”

“…In contrast to the nitrate-reducing and phototrophic Fe(II) oxidizers, marine microaerophilic Fe(II) oxidizers belong to the Zetaproteobacteria, as the ones that we found in the two different sediments from Aarhus Bay appear to be metabolically very restricted. All currently known isolates originate from ironrich environments and are obligate microaerophilic Fe(II) oxidizers (37,38,40,76). Although it was found that they carry the genes for nitrate reduction (75,103), there is so far no evidence from growth experiments that they can actually live by that type of metabolism.…”

“…This is the first time that the coexistence of all three metabolic types of Fe(II) oxidizers in the same habitat has been demonstrated, and we even identified members of these groups in enrichment cultures (see below). Marine microaerophilic Fe(II) oxidizers have so far been isolated only from deep-sea hydrothermal-vent systems or other marine habitats with elevated Fe(II) concentrations (18,38,75,76). Marine photoferrotrophs have been isolated from only one field site, i.e., a tidal mud flat in the German Wadden Sea by Straub et al (43).…”

Genomic insights into the uncultivated marine Zetaproteobacteria at Loihi Seamount

“…An operational taxonomic unit (OTU) was defined as a group of sequences with 97% sequence similarity to each other. These sequences were compared with reference sequences from McAllister et al (2011) to determine which global OTU these sequences correlated with.…”

“…To date, the Zetaproteobacteria have only been identified in habitats with high ferrous iron concentrations. Within this context, they have been detected in a wide range of environments from hydrothermal vent sites, such as Loihi Seamount, where they can dominate the microbial community (Rassa et al, 2009;Emerson and Moyer, 2010;McAllister et al, 2011;Fleming et al, 2013), to coastal environments, where they may be involved in biocorrosion of steel structures such as ships and pilings (Dang et al, 2011;McBeth et al, 2011).…”