Santelli Cara M.

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Santelli
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Cara M.
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  • Article
    Microbial- and thiosulfate-mediated dissolution of mercury sulfide minerals and transformation to gaseous mercury
    (Frontiers Media, 2015-06-23) Vazquez-Rodriguez, Adiari I. ; Hansel, Colleen M. ; Zhang, Tong ; Lamborg, Carl H. ; Santelli, Cara M. ; Webb, Samuel M. ; Brooks, Scott C.
    Mercury (Hg) is a toxic heavy metal that poses significant environmental and human health risks. Soils and sediments, where Hg can exist as the Hg sulfide mineral metacinnabar (β-HgS), represent major Hg reservoirs in aquatic environments. Metacinnabar has historically been considered a sink for Hg in all but severely acidic environments, and thus disregarded as a potential source of Hg back to aqueous or gaseous pools. Here, we conducted a combination of field and laboratory incubations to identify the potential for metacinnabar as a source of dissolved Hg within near neutral pH environments and the underpinning (a)biotic mechanisms at play. We show that the abundant and widespread sulfur-oxidizing bacteria of the genus Thiobacillus extensively colonized metacinnabar chips incubated within aerobic, near neutral pH creek sediments. Laboratory incubations of axenic Thiobacillus thioparus cultures led to the release of metacinnabar-hosted Hg(II) and subsequent volatilization to Hg(0). This dissolution and volatilization was greatly enhanced in the presence of thiosulfate, which served a dual role by enhancing HgS dissolution through Hg complexation and providing an additional metabolic substrate for Thiobacillus. These findings reveal a new coupled abiotic-biotic pathway for the transformation of metacinnabar-bound Hg(II) to Hg(0), while expanding the sulfide substrates available for neutrophilic chemosynthetic bacteria to Hg-laden sulfides. They also point to mineral-hosted Hg as an underappreciated source of gaseous elemental Hg to the environment.
  • Article
    Mn oxide formation by phototrophs: spatial and temporal patterns, with evidence of an enzymatic superoxide-mediated pathway
    (Nature Research, 2019-12-03) Chaput, Dominique L. ; Fowler, Alexandré J. ; Seo, Onyou ; Duhn, Kelly ; Hansel, Colleen M. ; Santelli, Cara M.
    Manganese (Mn) oxide minerals influence the availability of organic carbon, nutrients and metals in the environment. Oxidation of Mn(II) to Mn(III/IV) oxides is largely promoted by the direct and indirect activity of microorganisms. Studies of biogenic Mn(II) oxidation have focused on bacteria and fungi, with phototrophic organisms (phototrophs) being generally overlooked. Here, we isolated phototrophs from Mn removal beds in Pennsylvania, USA, including fourteen Chlorophyta (green algae), three Bacillariophyta (diatoms) and one cyanobacterium, all of which consistently formed Mn(III/IV) oxides. Isolates produced cell-specific oxides (coating some cells but not others), diffuse biofilm oxides, and internal diatom-specific Mn-rich nodules. Phototrophic Mn(II) oxidation had been previously attributed to abiotic oxidation mediated by photosynthesis-driven pH increases, but we found a decoupling of Mn oxide formation and pH alteration in several cases. Furthermore, cell-free filtrates of some isolates produced Mn oxides at specific time points, but this activity was not induced by Mn(II). Manganese oxide formation in cell-free filtrates occurred via reaction with the oxygen radical superoxide produced by soluble extracellular proteins. Given the known widespread ability of phototrophs to produce superoxide, the contribution of phototrophs to Mn(II) oxidation in the environment may be greater and more nuanced than previously thought.
  • Article
    Mechanisms of manganese(II) oxidation by filamentous ascomycete fungi vary with species and time as a function of secretome composition
    (Frontiers Media, 2021-02-10) Zeiner, Carolyn A. ; Purvine, Samuel O. ; Zink, Erika M. ; Wu, Si ; Pasa-Tolic, Ljiljana ; Chaput, Dominique L. ; Santelli, Cara M. ; Hansel, Colleen M.
    Manganese (Mn) oxides are among the strongest oxidants and sorbents in the environment, and Mn(II) oxidation to Mn(III/IV) (hydr)oxides includes both abiotic and microbially-mediated processes. While white-rot Basidiomycete fungi oxidize Mn(II) using laccases and manganese peroxidases in association with lignocellulose degradation, the mechanisms by which filamentous Ascomycete fungi oxidize Mn(II) and a physiological role for Mn(II) oxidation in these organisms remain poorly understood. Here we use a combination of chemical and in-gel assays and bulk mass spectrometry to demonstrate secretome-based Mn(II) oxidation in three phylogenetically diverse Ascomycetes that is mechanistically distinct from hyphal-associated Mn(II) oxidation on solid substrates. We show that Mn(II) oxidative capacity of these fungi is dictated by species-specific secreted enzymes and varies with secretome age, and we reveal the presence of both Cu-based and FAD-based Mn(II) oxidation mechanisms in all 3 species, demonstrating mechanistic redundancy. Specifically, we identify candidate Mn(II)-oxidizing enzymes as tyrosinase and glyoxal oxidase in Stagonospora sp. SRC1lsM3a, bilirubin oxidase in Stagonospora sp. and Paraconiothyrium sporulosum AP3s5-JAC2a, and GMC oxidoreductase in all 3 species, including Pyrenochaeta sp. DS3sAY3a. The diversity of the candidate Mn(II)-oxidizing enzymes identified in this study suggests that the ability of fungal secretomes to oxidize Mn(II) may be more widespread than previously thought.
  • Article
    Comparative analysis of secretome profiles of manganese(II)-oxidizing Ascomycete fungi
    (Public Library of Science, 2016-07-19) Zeiner, Carolyn A. ; Purvine, Samuel O. ; Zink, Erika M. ; Pasa-Tolic, Ljiljana ; Chaput, Dominique L. ; Haridas, Sajeet ; Wu, Si ; LaButti, Kurt ; Grigoriev, Igor V. ; Henrissat, Bernard ; Santelli, Cara M. ; Hansel, Colleen M.
    Fungal secretomes contain a wide range of hydrolytic and oxidative enzymes, including cellulases, hemicellulases, pectinases, and lignin-degrading accessory enzymes, that synergistically drive litter decomposition in the environment. While secretome studies of model organisms such as Phanerochaete chrysosporium and Aspergillus species have greatly expanded our knowledge of these enzymes, few have extended secretome characterization to environmental isolates or conducted side-by-side comparisons of diverse species. Thus, the mechanisms of carbon degradation by many ubiquitous soil fungi remain poorly understood. Here we use a combination of LC-MS/MS, genomic, and bioinformatic analyses to characterize and compare the protein composition of the secretomes of four recently isolated, cosmopolitan, Mn(II)-oxidizing Ascomycetes (Alternaria alternata SRC1lrK2f, Stagonospora sp. SRC1lsM3a, Pyrenochaeta sp. DS3sAY3a, and Paraconiothyrium sporulosum AP3s5-JAC2a). We demonstrate that the organisms produce a rich yet functionally similar suite of extracellular enzymes, with species-specific differences in secretome composition arising from unique amino acid sequences rather than overall protein function. Furthermore, we identify not only a wide range of carbohydrate-active enzymes that can directly oxidize recalcitrant carbon, but also an impressive suite of redox-active accessory enzymes that suggests a role for Fenton-based hydroxyl radical formation in indirect, non-specific lignocellulose attack. Our findings highlight the diverse oxidative capacity of these environmental isolates and enhance our understanding of the role of filamentous Ascomycetes in carbon turnover in the environment.
  • Article
    Profiling microbial communities in manganese remediation systems treating coal mine drainage
    (American Society for Microbiology, 2015-01-16) Chaput, Dominique L. ; Hansel, Colleen M. ; Burgos, William D. ; Santelli, Cara M.
    Water discharging from abandoned coal mines can contain extremely high manganese levels. Removing this metal is an ongoing challenge. Passive Mn(II) removal beds (MRBs) contain microorganisms that oxidize soluble Mn(II) to insoluble Mn(III/IV) minerals, but system performance is unpredictable. Using amplicon pyrosequencing, we profiled the bacterial, fungal, algal and archaeal communities in four variably-performing MRBs in Pennsylvania to determine whether they differed among MRBs and from surrounding soil, and to establish the relative abundance of known Mn(II)-oxidizers. Archaea were not detected; PCRs with archaeal primers returned only non-target bacterial sequences. Fungal taxonomic profiles differed starkly between sites that remove the majority of influent Mn and those that do not, with the former dominated by Ascomycota (mostly Dothideomycetes) and the latter by Basidiomycota (almost entirely Agaricomycetes). Taxonomic profiles for the other groups did not differ significantly between MRBs, but OTU-based analyses showed significant clustering by MRB with all four groups (p<0.05). Soil samples clustered separately from MRBs in all groups except fungi, whose soil samples clustered loosely with their respective MRB. Known Mn(II) oxidizers accounted for a minor proportion of bacterial sequences (up to 0.20%) but a greater proportion of fungal sequences (up to 14.78%). MRB communities are more diverse than previously thought, and more organisms may be capable of Mn(II) oxidation than are currently known.
  • Thesis
    Geomicrobiology of the ocean crust : the phylogenetic diversity, abundance, and distribution of microbial communities inhabiting basalt and implications for rock alteration processes
    (Massachusetts Institute of Technology and Woods Hole Oceanographic Institution, 2007-06) Santelli, Cara M.
    Basaltic ocean crust has the potential to host one of the largest endolithic communities on Earth. This portion of the biosphere, however, remains largely unexplored. In this study, we utilize molecular biological, microscopic, and geochemical tools to gain a better understanding of the geomicrobiology of the ocean crust. Specifically, we examine the phylogenetic diversity of microorganisms inhabiting basaltic lavas, the activities and abundances of these microorganisms, the spatial extent of the biosphere, and the potential effect that microbial activity has on the geochemistry of the ocean crust and overlying water column. Our study demonstrates that young, fresh volcanic lavas near mid-ocean ridges host an incredibly diverse and dense population of microorganisms dominated by Bacteria, quite distinct from the microbial communities found in surrounding deep seawater and hydrothermal vents. Furthermore, these communities may contribute to the elemental cycling of Fe, S, Mn, N, and C in this environment. The inability to definitively identify microorganisms in drill-cores of old (> 15 Ma) ocean crust, however, implies that these once prolific communities may become scarce as the crust ages and moves further away from the ridge axis. Finally, we provide evidence suggesting that these communities are fueled by oxidative alteration reactions occurring in the basaltic crust.