Competitive ligand exchange between Cu–humic acid complexes and methanobactin

Abstract

Copper has been found to play a key role in the physiology of methanotrophic micro-organisms, and methane oxidation may critically depend on the availability of Cu. In natural environments, such as soils, sediments, peat bogs, and surface waters, the presence of natural organic matter (NOM) can control the bioavailability of Cu by forming strong metal complexes. To promote Cu acquisition, methanotrophs exude methanobactin, a ligand known to have a high affinity for Cu. In this study, the capability of methanobactin for Cu acquisition from NOM was investigated using humic acid (HA) as a model substance. The kinetics of ligand exchange between Cu-HA and methanobactin was observed by UV-vis spectroscopy, and the speciation of Cu bound to methanobactin was determined by size-exclusion chromatography coupled to an ICP-MS. The results showed that Cu was mobilized from HA by a fast ligand exchange reaction following a second-order rate law with first-order kinetics for both methanobactin and Cu-HA complexes. The reaction rates decreased with decreasing temperature. Equilibrium experiments indicated that methanobactin was not sorbed to HA and proved that methanobactin is competitive with HA for Cu binding by forming strong 1:1 Cu-methanobactin complexes. Consequently, our results demonstrate that methanobactin can efficiently acquire Cu in organic-rich environments.

Chalkophores

“…These observations are consistent with a major role for Mbn in liberating copper from organic-rich environments with a near-neutral pH, such as peatlands, rice paddies, lake sediments, and soils, which are some of the common habitats for methanotrophs (51, 52). Mbn can also bind metals other than copper.…”

“…Due to its high copper affinity, Mbn can extract copper from a wide range of otherwise biounavailable mineral sources, including borosilicate glass and humic acid species (50, 51). These observations are consistent with a major role for Mbn in liberating copper from organic-rich environments with a near-neutral pH, such as peatlands, rice paddies, lake sediments, and soils, which are some of the common habitats for methanotrophs (51, 52).…”

Metallophores and Trace Metal Biogeochemistry

“…Because metallophores are exuded to increase the bioavailability of trace metals, the principal process in which they are involved is the complexation and mobilization of metals from environmental reactive compounds. For example, metallophores have been demonstrated to complex adsorbed metals through a ligand exchange reaction (Pesch et al 2013) and to solubilize metal ions from mineral phases via ligand-promoted dissolution (Kraemer 2004). …”

“…In a recent study, it was shown that Cu exchange reactions between humic substances and methanobactin were rapid, but that the rate decreased with decreasing temperature and Cu concentration. Therefore, it is conceivable that methanotrophic Cu acquisition in organic-rich systems with low Cu concentrations may be kinetically limited by such exchange reactions (Pesch et al 2013). Clearly, the understanding of chalkophore geochemistry in natural systems remains a challenge for future research.…”

Methanobactins: Maintaining copper homeostasis in methanotrophs and beyond

“…Mbns slightly affect copper affinity (23,25). The Cu(I) affinity is high enough that Mbn can liberate bio-unavailable copper from sources ranging from humic acids (30) to minerals (31) to borosilicate glass (32,33). Although Mbns bind Cu(II) with lower affinity, generally calculated to be 10 11 -10 14 M -1 (25), binding is reductive, with conversion to Cu(I) within the first 10 min via an unknown mechanism, as confirmed by electron paramagnetic resonance and X-ray absorption spectroscopies (27,29,34,35).…”