Abstract
Microbes form mats with architectures that promote efficient metabolism within a particular physicochemical environment, thus studying mat structure helps us understand ecophysiology. Despite much research on chemolithotrophic Fe-oxidizing bacteria, Fe mat architecture has not been visualized because these delicate structures are easily disrupted. There are striking similarities between the biominerals that comprise freshwater and marine Fe mats, made by Beta- and Zetaproteobacteria, respectively. If these biominerals are assembled into mat structures with similar functional morphology, this would suggest that mat architecture is adapted to serve roles specific to Fe oxidation. To evaluate this, we combined light, confocal, and scanning electron microscopy of intact Fe microbial mats with experiments on sheath formation in culture, in order to understand mat developmental history and subsequently evaluate the connection between Fe oxidation and mat morphology. We sampled a freshwater sheath mat from Maine and marine stalk and sheath mats from Loihi Seamount hydrothermal vents, Hawaii. Mat morphology correlated to niche: stalks formed in steeper O2 gradients while sheaths were associated with low to undetectable O2 gradients. Fe-biomineralized filaments, twisted stalks or hollow sheaths, formed the highly porous framework of each mat. The mat-formers are keystone species, with nascent marine stalk-rich mats comprised of novel and uncommon Zetaproteobacteria. For all mats, filaments were locally highly parallel with similar morphologies, indicating that cells were synchronously tracking a chemical or physical cue. In the freshwater mat, cells inhabited sheath ends at the growing edge of the mat. Correspondingly, time lapse culture imaging showed that sheaths are made like stalks, with cells rapidly leaving behind an Fe oxide filament. The distinctive architecture common to all observed Fe mats appears to serve specific functions related to chemolithotrophic Fe oxidation, including (1) removing Fe oxyhydroxide waste without entombing cells or clogging flow paths through the mat and (2) colonizing niches where Fe(II) and O2 overlap. This work improves our understanding of Fe mat developmental history and how mat morphology links to metabolism. We can use these results to interpret biogenicity, metabolism, and paleoenvironmental conditions of Fe microfossil mats, which would give us insight into Earth's Fe and O2 history.
Highlights
Microbial mats are intricately organized structures that provide functional advantage to their inhabitants (e.g., Stahl et al, 2013)
Following Zetaproteobacterial operational taxonomic units (OTUs) (ZOTU) designations outlined by McAllister et al (2011), we found the normally rare ZOTU6 dominating the Zetaproteobacterial community in one intact curd sample (434 of 857, or 50.6% of Zetaproteobacterial sequences), while another sample was dominated by three novel ZOTUs, designated here as new ZOTU N1, N2, and N3 (Supplemental Figure 1)
The work presented here clearly demonstrates that Fe-oxidizing bacteria (FeOB) produce organized microbial mats, rather than “Fe flocs,” as they are commonly referred to, since flocculation implies aggregation of cells and minerals after precipitation
Summary
Microbial mats are intricately organized structures that provide functional advantage to their inhabitants (e.g., Stahl et al, 2013). Chemolithotrophic microaerophilic Fe-oxidizing bacteria (FeOB) are well known for creating distinctive orange-rust colored mats where ferrous-rich fluids flow into oxygenated surface water (e.g., groundwater seeps, hydrothermal vents; Harder, 1919; Ghiorse, 1984; Emerson et al, 2010) These mats are often referred to as “flocs,” and they break apart and flocculate, suggesting that coherence could result from random organization. The striking parallel between terrestrial Betaproteobacteria and marine Zetaproteobacteria suggests that the filament-based mat structure plays specific roles in promoting microbial Fe oxidation This would prove true if all types of filamentforming FeOB use their filaments to produce mats with similar architectures, despite the fact that stalk and sheath morphologies represent different O2 niches, distinct cell-mineral spatial relationships (Figure 1), and likely distinct genetic mechanisms. Coupled to field observations and geochemical measurements, we show that Fe mat structure appears to be a function of environmental niche and the distinct challenges of microbial Fe oxidation, including efficient Fe biomineralization without encrustation and maintaining position in Fe(II) and O2 gradients
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