Contribution of Microaerophilic Iron(II)-Oxidizers to Iron(III) Mineral Formation

Abstract

Neutrophilic microbial aerobic oxidation of ferrous iron (Fe­(II)) is restricted to pH-circumneutral environments characterized by low oxygen where microaerophilic Fe­(II)-oxidizing microorganisms successfully compete with abiotic Fe­(II) oxidation. However, accumulation of ferric (bio)­minerals increases competition by stimulating abiotic surface-catalyzed heterogeneous Fe­(II) oxidation. Here, we present an experimental approach that allows quantification of microbial and abiotic contribution to Fe­(II) oxidation in the presence or initial absence of ferric (bio)­minerals. We found that at 20 μM O2 and the initial absence of Fe­(III) minerals, an iron­(II)-oxidizing enrichment culture (99.6% similarity to Sideroxydans spp.) contributed 40% to the overall Fe­(II) oxidation within approximately 26 h and oxidized up to 3.6 × 10–15 mol Fe­(II) cell–1 h–1. Optimum O2 concentrations at which enzymatic Fe­(II) oxidation can compete with abiotic Fe­(II) oxidation ranged from 5 to 20 μM. Lower O2 levels limited biotic Fe­(II) oxidation, while at higher O2 levels abiotic Fe­(II) oxidation dominated. The presence of ferric (bio)­minerals induced surface-catalytic heterogeneous abiotic Fe­(II) oxidation and reduced the microbial contribution to Fe­(II) oxidation from 40% to 10% at 10 μM O2. The obtained results will help to better assess the impact of microaerophilic Fe­(II) oxidation on the biogeochemical iron cycle in a variety of environmental natural and anthropogenic settings.

Why do microbes make minerals?

“…The organic structures direct Fe(III) precipitation away from the cells, preventing their encrustation by iron minerals [Chan et al, 2011], a function that is further aided by specific mineral-repelling properties of the cell surface such as low charge and hydrophilicity [Saini and Chan, 2013]. In addition, sheaths and stalks appear to serve as attachment and support structures that help the microbes occupy niches where O 2 and Fe(II) gradients overlap [Chan et al, 2016a], an important requirement for these microaerophilic iron oxidizers [Emerson et al, 2010, Maisch et al, 2019 (Figure 3D). Indeed, when Mariprofundus ferrooxydans is grown in opposing O 2 and Fe(II) concentration gradients, their stalks, forming rigid holdfasts anchoring them to surfaces, grow directionally toward higher oxygen concentrations, allowing the bacteria (living at the end of stalks) to orient themselves within the redox gradient and colonize a narrow band with well-defined O 2 and Fe(II) conditions [Krepski et al, 2013] (Figure 3B).…”

Unraveling Fe(II)-oxidizing mechanisms in a facultative Fe(II) oxidizer Sideroxydans lithotrophicus ES-1 via culturing, transcriptomics, and RT-qPCR

“…Neutrophilic Fe(II)-oxidizing bacteria (FeOB) are increasingly found in a wide variety of terrestrial and marine environments (1)(2)(3)(4), often in suboxic zones where microaerophilic FeOB can successfully outcompete abiotic Fe(II) oxidation (5,6). In these environments, FeOB have the potential to affect many elemental cycles, notably carbon cycling as many neutrophilic FeOB are autotrophic and sequester organics in their biominerals (7,8).…”

Continuous cultivation of the lithoautotrophic nitrate-reducing Fe(II)-oxidizing culture KS in a chemostat bioreactor

“…Fe(II)-oxidizing bacteria at circumneutral pH use Fe(II) as an electron donor to reduce electron acceptors such as O2, CO2, or nitrate (Bryce et al, 2018). Microaerophilic Fe(II)oxidizing bacteria compete with abiotic Fe(II) oxidation at low O2-concentrations (Emerson and Moyer, 1997;Druschel et al, 2008;Maisch et al, 2019), while anaerobic phototrophic Fe(II)-oxidizers use light energy to reduce and fix CO2 (Widdel et al, 1993;Ehrenreich and Widdel, 1994). Finally, nitrate-reducing Fe(II)-oxidizing (NRFeOx) bacteria couple Fe(II) oxidation to the reduction of nitrate (NO3 -) in anoxic environments (Straub et al, 1996;Weber et al, 2006;Roden, 2012).…”