The Architecture of Iron Microbial Mats Reflects the Adaptation of Chemolithotrophic Iron Oxidation in Freshwater and Marine Environments

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.

Peeking under the Iron Curtain: Development of a Microcosm for Imaging the Colonization of Steel Surfaces by Mariprofundus sp. Strain DIS-1, an Oxygen-Tolerant Fe-Oxidizing Bacterium

“…This suggests that DIS-1 is a good representative of natural FeOB capable of colonizing steel surfaces. The behavior of DIS-1 growing on the coupon surface is also reminiscent of stalk-forming FeOB that grow at hydrothermal vents and are related to DIS-1 (41). In this case, zetaproteobacteria also produce loosely adherent mats on the surfaces of basaltic lava substrata around the vents (11).…”

“…It is likely that this is the natural habitat of DIS-1. A recent study that captured intact vent mats showed stalk-forming FeOB were early colonizers and the primary architect of these mats (41). Stalk formation occurred in a highly parallel fashion, such that the mat grew with a uniform directionality perpendicular to the rock face and showed remarkable temporal and spatial coordination in the formation of the intact microbial mat (41).…”

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

“…These results are in good agreement with the optical microscopy results from the Jan Mayen Si‐Fe mounds, which show that the preferred orientation of irregular stalks is localized. Microbial mats in natural hydrothermal environments are affected by shifting flow paths and changing redox gradients during progressive Fe‐oxyhydroxide precipitation (Chan, McAllister, et al, ) and are sporadically exposed to strong fluid flow (Bernis, Lowell, & Farough, ). These factors likely impact the directionality of the filamentous fabric by promoting both abrupt and gradual changes in filament orientation, explaining the confinement of aligned filaments to distinct domains.…”

Bringing microbial diversity into focus: high‐resolution analysis of iron mats from the Lō‘ihi Seamount

“…One common morphotype in mats that attaches to either sheaths or stalks is an organism that produces unique Y-shaped branched filaments (Chan et al, 2016). Since ferrous iron is assumed to be the primary energy source for both cosmopolitan and endemic strains, other traits may play a role in determining the successful ecological strategies of cosmopolitan Zetaproteobacteria.…”

“…The spatial resolution for collecting samples with the mat sampler was approximately 1 cm, either vertically or horizontally. Chemistry measurements were conducted using an in-situ electrochemical analyzer, ISEA, (ISEA-III, Analytical Instrument Systems, Flemington, NJ, USA) as described elsewhere (Chan et al, 2016). 1A).…”