Impacts of sulfonic acids on fungal manganese oxide production

Hinkle, Margaret A.G.; Post, Jeffrey E.; Peralta, Javier; Santelli, Cara M.

doi:10.1016/j.gca.2022.11.032

Impacts of sulfonic acids on fungal manganese oxide production

Journal Article · Fri Dec 02 00:00:00 EST 2022 · Geochimica et Cosmochimica Acta

DOI:https://doi.org/10.1016/j.gca.2022.11.032· OSTI ID:2423470

Hinkle, Margaret A.G. ^[1]; Post, Jeffrey E. ^[2]; Peralta, Javier ^[3]; Santelli, Cara M. ^[4]

Smithsonian Institute, Washington, DC (United States); Washington and Lee University, Lexington, VA (United States)
Smithsonian Institute, Washington, DC (United States)
Washington and Lee University, Lexington, VA (United States); Stanford Univ., CA (United States)
Univ. of Minnesota, Minneapolis, MN (United States)

Microbial manganese (Mn) oxidation plays a critical role in Mn(III/IV) oxide formation in modern day environmental systems. These oxidation processes and resulting biominerals are sensitive to aqueous conditions, such as pH and dissolved constituent concentrations. With Mn and sulfur (S) biogeochemical cycling closely linked in many environmental systems, and dissolved organic sulfur comprising a substantial pool of total sulfur in several environments, the impact of dissolved organic sulfur compounds on Mn redox processes is important to consider. Sulfonic acids, environmentally ubiquitous organosulfur compounds, play substantial roles in S cycling in many natural and contaminated systems. Research to assess the effects of these abundant sulfonic acids on Mn biogeochemical cycling, microbial Mn oxidation processes, and Mn biominerals is needed for understanding and predicting the impact of coupled S and Mn biogeochemical cycles, particularly in environments with dynamic redox gradients or in anthropogenically contaminated systems. Further, with research on microbial and abiotic Mn oxidation processes often using aminosulfonic acids to control pH, understanding the impact of such sulfonic acids on microbial Mn oxidation processes is critical. Several recent studies found that commonly used zwitterionic N substituted aminosulfonic acids, known as Good’s buffers, such as HEPES and MES, can alter abiotic birnessite sheet structures. Here we investigate the impact of two sulfonic acids with broad applications to natural and contaminated sites as well as laboratory settings (HEPES and MES) on fungal Mn oxidation relative to a carbonate buffer and a buffer-free control by three Ascomycete fungi known to oxidize Mn(II): Stagonospora sp. SRC1lsM3a, Paraphaeosphaeria sporulosa AP3s5–JAC2a, and Plectosphaerella cucumerina DS2psM2a2. Structural analyses of the products show that sulfonic acids promote Mn oxidation by P. cucumerina, producing hexagonally symmetric phyllomanganates analogous to hexagonal birnessite or c–disordered H⁺ birnessite [(Ca,Na,K)(Mn⁴⁺,Mn³⁺,$$\square$$)O₂ nH₂O], with solid–associated Mn(II) bound to vacancy sites and biomass, while in their absence almost all Mn remains as either aqueous Mn(II) or solid–associated Mn(II) bound to biomass. In contrast, sulfonic acids exert the opposite effect on Mn oxidation by P. sporulosa, with their presence suppressing Mn(II) oxidation to Mn(IV), likely leading to the formation of mycogenic bixbyite (Mn³⁺₂O₃) while the buffer–free control forms a poorly crystalline phyllo- or tectomanganate. Meanwhile, all treatments exert a minimal effect on Mn(II) uptake from solution and Mn oxidation with Stagonospora sp., with all experimental systems and controls forming poorly crystalline, hexagonally symmetric phyllomanganates. The fact that the sulfonic acids here studied exert similar effects on Mn oxidation, but substantially different effects for each fungus, suggests they affect Mn oxidation via mechanistically similar pathways that are likely dependent on interactions with fungal exudates (which vary from species to species) or specific fungal Mn oxidation processes. Interestingly, for all fungi, MES increases Mn(III) in the resulting biominerals, while the carbonate buffer consistently decreases Mn(III). Further, these results clearly demonstrate that sulfonic acids not only alter Mn oxide structures, as has been previously noted in abiotic studies, but can interfere with Mn oxidation reactions themselves, highlighting the incredible sensitivity of both Mn oxide structures and the Mn oxidation process to the aqueous environment.

View Accepted Manuscript (DOE)

Research Organization:: Argonne National Laboratory (ANL), Argonne, IL (United States). Advanced Photon Source (APS); SLAC National Accelerator Laboratory (SLAC), Menlo Park, CA (United States)

Sponsoring Organization:: National Science Foundation (NSF); USDOE Office of Science (SC)

Grant/Contract Number:: AC02-06CH11357; AC02-76SF00515

OSTI ID:: 2423470

Journal Information:: Geochimica et Cosmochimica Acta, Journal Name: Geochimica et Cosmochimica Acta Journal Issue: C Vol. 341; ISSN 0016-7037

Publisher:: Elsevier; The Geochemical Society; The Meteoritical SocietyCopyright Statement

Country of Publication:: United States

Language:: English

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58 GEOSCIENCES
59 BASIC BIOLOGICAL SCIENCES
Birnessite
Bixbyite
Fungi
Manganese biomineralization
Manganese oxidizing fungi
Mn oxidation
Mycogenic manganese oxides
Phyllomanganates
Redox reactions
Sulfonic acids

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