Population Structure of Manganese-Oxidizing Bacteria in Stratified Soils and Properties of Manganese Oxide Aggregates under Manganese–Complex Medium Enrichment

Abstract

Manganese-oxidizing bacteria in the aquatic environment have been comprehensively investigated. However, little information is available about the distribution and biogeochemical significance of these bacteria in terrestrial soil environments. In this study, stratified soils were initially examined to investigate the community structure and diversity of manganese-oxidizing bacteria. Total 344 culturable bacterial isolates from all substrata exhibited Mn(II)-oxidizing activities at the range of 1 µM to 240 µM of the equivalent MnO2. The high Mn(II)-oxidizing isolates (>50 mM MnO2) were identified as the species of phyla Actinobacteria, Firmicutes and Proteobacteria. Seven novel Mn(II)-oxidizing bacterial genera (species), namely, Escherichia, Agromyces, Cellulomonas, Cupriavidus, Microbacterium, Ralstonia, and Variovorax, were revealed via comparative phylogenetic analysis. Moreover, an increase in the diversity of soil bacterial community was observed after the combined enrichment of Mn(II) and carbon-rich complex. The phylogenetic classification of the enriched bacteria represented by predominant denaturing gradient gel electrophoresis bands, was apparently similar to culturable Mn(II)-oxidizing bacteria. The experiments were further undertaken to investigate the properties of the Mn oxide aggregates formed by the bacterial isolates with high Mn(II)-oxidizing activity. Results showed that these bacteria were closely encrusted with their Mn oxides and formed regular microspherical aggregates under prolonged Mn(II) and carbon-rich medium enrichment for three weeks. The biotic oxidation of Mn(II) to Mn(III/IV) by these isolates was confirmed by kinetic examinations. X-ray diffraction assays showed the characteristic peaks of several Mn oxides and rhodochrosite from these aggregates. Leucoberbelin blue tests also verified the Mn(II)-oxidizing activity of these aggregates. These results demonstrated that Mn oxides were formed at certain amounts under the enrichment conditions, along with the formation of rhodochrosite in such aggregates. Therefore, this study provides insights into the structure and diversity of soil-borne bacterial communities in Mn(II)-oxidizing habitats and supports the contribution of soil-borne Mn(II)-oxidizing bacteria to Mn oxide mineralization in soils.

Microbial community composition of a household sand filter used for arsenic, iron, and manganese removal from groundwater in Vietnam

“…For example; two Mn(II)-oxidizing bacterial cultures have been isolated from an alfisol soil (Sullivan and Koppi, 1993) and phylogenetically diverse bacterial and archaeal communities have been found in association with ferromanganese nodules in soil and sediment samples (Stein et al, 2001;Carmichael et al, 2013;Tully and Heidelberg, 2013). However, very limited information is available about microbial mechanisms and microorganisms mediating Mn oxidation in soils (He et al, 2008;Yang et al, 2013). Consistently, we did not identify any OTUs related to known Mn-oxidizing bacteria in the pyrosequencing libraries of the sand filter samples.…”

Changes in morphology and metabolism enable Mn‐oxidizing bacteria from mid‐oceanic ridge environment to counter metal‐induced stress

“…Nevertheless, these observations indicate that Mn (II) oxidizing bacteria tested in the present study were capable of depositing Mn‐oxides as microspherical aggregates. The difference in size of microspherical aggregates could be due to the different Mn (II) oxidizing activities of the isolates . As observed in the present study, Yang et al have demonstrated that Mn (II) oxidizing bacteria isolated from stratified soils were encrusted with Mn‐oxides and formed regular microspherical aggregates under prolonged (∼3 weeks) exposure to Mn(II) and carbon‐rich medium enrichment.…”

“…The difference in size of microspherical aggregates could be due to the different Mn (II) oxidizing activities of the isolates . As observed in the present study, Yang et al have demonstrated that Mn (II) oxidizing bacteria isolated from stratified soils were encrusted with Mn‐oxides and formed regular microspherical aggregates under prolonged (∼3 weeks) exposure to Mn(II) and carbon‐rich medium enrichment. Striking resemblance of microspherical aggregate formations were observed when compared to SEM images of Fe–Mn oxide deposits (intermediate layer) from the Lau Basin (Figure ).…”

Profiling Microbial Communities in Manganese Remediation Systems Treating Coal Mine Drainage

“…This widespread, highly diverse phylum is dominant in many environments, notably soils (including the four control soil samples in this study, although at a significantly lower abundance than that in the MRBs). It also encompasses numerous confirmed examples of Mn(II) oxidation in the Alpha-, Beta-, Gamma-, and Deltaproteobacteria (10,11,14,15,24,55). Indeed, many of the model Mn(II)-oxidizing bacteria used to elucidate mechanisms of oxidation belong to this phylum (23)(24)(25)58).…”

“…Mineral surface-catalyzed Mn(II) oxidation was shown to occur in simulated CMD treatment bioreactors, although microbial activity dominated the oxidation of Mn(II) to Mn(III/IV) oxides under certain treatment conditions (2). A diversity of bacteria (10)(11)(12)(13)(14)(15) and fungi (12,(15)(16)(17)(18), isolated from a range of aquatic and terrestrial environments, are known to oxidize Mn(II) when grown in pure culture, although not as an energy-conserving process but rather as a side reaction of unknown physiological basis. The remediation of Mn-contaminated waters is thought to rely largely on such organisms.…”