Distribution Patterns of Iron-Oxidizing Zeta- and Beta-Proteobacteria From Different Environmental Settings at the Jan Mayen Vent Fields

Abstract

Iron oxidizers are widespread in marine environments and play an important role in marine iron cycling. However, little is known about the overall distribution of iron oxidizers within hydrothermal systems, including settings with little hydrothermal activity. Moreover, the extent to which different phylogenetic groups of iron oxidizers exhibit niche specialization toward different environmental settings, remains largely unknown. Obtaining such knowledge is critical to unraveling the impact of the activity of iron oxidizers and how they are adapted. Here, we used 16S rRNA sequencing to characterize the distribution of iron oxidizers in different environmental settings within the Jan Mayen hydrothermal vent fields (JMVFs). Putative iron oxidizers affiliated to Zetaproteobacteria and Betaproteobacteria were detected within iron mounds, bottom seawater, basalt surfaces, and surface layers of sediments. The detected iron oxidizers were compared to sequence types previously observed in patchily distributed iron mats associated with diffuse venting at the JMVFs. Most OTUs of iron oxidizers reoccurred under different environmental settings, suggesting a limited degree of niche specialization. Consequently, most of the detected iron oxidizers seem to be generalists with a large habitat range. Our study highlights the importance of gathering information about the overall distribution of iron oxidizers in hydrothermal systems to fully understand the role of this metabolic group regarding cycling of iron. Furthermore, our results provide further evidence of the presence of iron-oxidizing members of Betaproteobacteria in marine environments.

Keywords: Betaproteobacteria; Zetaproteobacteria; hydrothermal systems; iron oxidizers; microbial ecology.

FIGURE 1

Location of the Jan Mayen vent fields (JMVFs) and images of sampling strategies in this study using a remotely operated vehicle. (A) Map showing the location of the JMVFs. (B) Sampling an iron mat using a hydraulic suction device. (C) Sampling of an iron mound using a shovel-box. Basalt samples were collected with a manipulator arm claw. (D) Sampling of sediments using push-cores. (E) Sampling of deep-sea water using a hydraulic suction device.

FIGURE 2

Microbial composition on class level of 34 JMVF samples from five different habitats: Fe mat (Mat), Fe mound (IM), basalts (Bas), sediment (Sed), and deep-sea water (SW). Relative abundances of FeOζ (Zetaproteobacteria) and FeOβ (Gallionella, Sideroxydans, and Leptothrix) are indicated.

FIGURE 3

(A) Ward.D2 cluster analysis of all microbial communities from the five sampled JMVF habitats. These samples were pooled (highlighted with color) and, consequently, (B) subjected to a new cluster analysis. (C) NMDS plot situating the pooled samples and the OTU number of the detected iron oxidizers (comprising FeOζ and FeOβ). The FeOζ OTU and FeOβ OTU numbers are scaled to their overall abundance within the entire community.

FIGURE 4

Bubble plot showing the relative abundances of ZetaOtus (FeOζ) and BetaOTUs (FeOβ) across the different habitats (Mat, iron mat; IM, iron mound; Sed, sediment; Bas, basalts; SW, deep-sea water). Samples were pooled as in Figure 3 and clustered by the ward.D2 method using Bray-Curtis distances. Iron oxidizers were phylogenetically clustered by maximum-likelihood. Bubble radii are scaled to their relative abundance within the entire microbial community. Relative fractions >0.1 are indicated in white. Scale bar represents 0.02 substitutions/site.

FIGURE 5

Maximum-likelihood phylogenetic tree of FeOβ from marine (cyan) and freshwater (brown) environments from around the world. Sequences from the JMVFs (this study) are shown in bold. Scale bar represents 0.03 substitutions/site.