The Architecture of Iron Microbial Mats Reflects the Adaptation of Chemolithotrophic Iron Oxidation in Freshwater and Marine Environments
Year: 2016
Type: article
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.
Source: Frontiers in Microbiology
Language: English
Subfield: Ecology
Field: Environmental Science
Domain: Physical Sciences
SDG: Life below water
Open Access status: gold
Estimated APC paid: $3,801
Awards: THE GUIDING PRINCIPLES OF THE DELAWARE SPACE GRANT COLLEGE (DESGC) PROGRAM ARE AS FOLLOWS: REASON FOR DESGC'S EXISTENCE: TO SERVE THE PEOPLE OF THE S, EARTH'S HISTORY IS INEXTRICABLY LINKED TO THE REDOX STATES OF IRON AND THE FORMATION OF O2 . BOTH HAVE REACTED OVER TIME, AS EVIDENCED BY BANDED IRON, G4141369891, Collaborative Research: Ecology of microbial mats at seamount associated Fe-rich hydrothermal vent systems, Collaborative Research: Ecology of microbial mats at seamount associated Fe-rich hydrothermal vent systems
OpenAlex ID: W2415933542