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Nealson, Kenneth H.

Publications and source records attributed to Nealson, Kenneth H..

At least 19 records
All sourcesNASA NTRSDOE OSTI
DOE OSTI2024

Large-scale prediction of outer-membrane multiheme cytochromes uncovers hidden diversity of electroactive bacteria and underlying pathways

Multi-heme cytochromes (MHCs), together with accessory proteins like porins and periplasmic cytochromes, enable microbes to transport electrons between the cytoplasmic membrane and extracellular substrates (e.g., minerals, electrodes, other cells). Extracellular electron transfer (EET) has been described in multiple systems; yet, the broad phylogenetic and mechanistic diversity of these pathways is less clear. One commonality in EET-capable systems is the involvement of MHCs, in the form of porin-cytochrome complexes, pili-like cytochrome polymers, and lipid-anchored extracellular cytochromes. Here, we put forth MHCscan—a software tool for identifying MHCs and identifying potential EET capability. Using MHCscan, we scanned ~60,000 bacterial and 2,000 archaeal assemblies, and identify a diversity of MHCs, many of which represent enzymes with no known function, and many found within organisms not previously known to be electroactive. In total, our scan identified ~1,400 unique enzymes, each encoding more than 10 heme-binding motifs. In our analysis, we also find evidence for modularity and flexibility in MHC-dependent EET pathways, and suggest that MHCs may be far more common than previously recognized, with many facets yet to be discovered. We present MHCscan as a lightweight and user-friendly software tool that is freely available: https://github.com/Arkadiy-Garber/MHCscan.

59 BASIC BIOLOGICAL SCIENCES↗
DOE OSTI2023

Insights into the physiological and genomic characterization of three bacterial isolates from a highly alkaline, terrestrial serpentinizing system

The terrestrial serpentinite-hosted ecosystem known as “The Cedars” is home to a diverse microbial community persisting under highly alkaline (pH ~ 12) and reducing (Eh < -550 mV) conditions. This extreme environment presents particular difficulties for microbial life, and efforts to isolate microorganisms from The Cedars over the past decade have remained challenging. Herein, we report the initial physiological assessment and/or full genomic characterization of three isolates: Paenibacillus sp. Cedars (‘Paeni-Cedars’), Alishewanella sp. BS5-314 (‘Ali-BS5-314’), and Anaerobacillus sp. CMMVII (‘Anaero-CMMVII’). Paeni-Cedars is a Gram-positive, rod-shaped, mesophilic facultative anaerobe that grows between pH 7–10 (minimum pH tested was 7), temperatures 20–40°C, and 0–3% NaCl concentration. The addition of 10–20 mM CaCl 2 enhanced growth, and iron reduction was observed in the following order, 2-line ferrihydrite > magnetite > serpentinite ~ chromite ~ hematite. Genome analysis identified genes for flavin-mediated iron reduction and synthesis of a bacillibactin-like, catechol-type siderophore. Ali-BS5-314 is a Gram-negative, rod-shaped, mesophilic, facultative anaerobic alkaliphile that grows between pH 10–12 and temperatures 10–40°C, with limited growth observed 1–5% NaCl. Nitrate is used as a terminal electron acceptor under anaerobic conditions, which was corroborated by genome analysis. The Ali-BS5-314 genome also includes genes for benzoate-like compound metabolism. Anaero-CMMVII remained difficult to cultivate for physiological studies; however, growth was observed between pH 9–12, with the addition of 0.01–1% yeast extract. Anaero-CMMVII is a probable oxygen-tolerant anaerobic alkaliphile with hydrogenotrophic respiration coupled with nitrate reduction, as determined by genome analysis. Based on single-copy genes, ANI, AAI and dDDH analyses, Paeni-Cedars and Ali-BS5-314 are related to other species (P. glucanolyticus and A. aestuarii, respectively), and Anaero-CMMVII represents a new species. The characterization of these three isolates demonstrate the range of ecophysiological adaptations and metabolisms present in serpentinite-hosted ecosystems, including mineral reduction, alkaliphily, and siderophore production.

59 BASIC BIOLOGICAL SCIENCES↗
DOE OSTI2022

Microbial community diversity changes during voltage reversal repair in a 12-unit microbial fuel cell

Microbial fuel cell stacks (MFC-Stack) are often confronted with voltage reversals, likely due to an interplay between microbial community dynamics and insufficient electric circuit balancing. Herein, we provide new insight into voltage reversals by examining the microbiomes of twelve MFC units of a 12-liter Pilot-MFC-Stack during repair. Different biofilm repair methods (self-healing, electrostimulation, and re-acclimatization upon cross-inoculation) were used to evaluate the microbial community response. In addition, MFC-Stack simulation was performed based on Kirchhoff’s Second Law to predict values for source potentials and post-evaluate internal resistances. Analysis of the 16S rRNA amplicon sequencing data suggests that the biofilm repair methods could slowly heal damaged biofilms. Notably, severely voltage reversed MFC units had low electrogen relative abundances (18%) and positive anode potentials, while strong bioanodes and contained more than 50% electrogens and had negative anode potentials. Between-community analyses (beta diversity ordination and multinomial regression) of the voltage reversed MFC units revealed differences among biofilms in contrast to healthy/strong MFC units. Permutational multivariate analysis of variance (PERMANOVA) confirmed that reversed biofilms were, indeed, significantly (p < 0.05) different from stronger ones. Overall, these analyses demonstrated the utility of combining electrotechnical and microbial community analyses, especially beta diversity ordination and multinomial regression, to understand problematic MFC units and the potential success of a biofilm repair method. Finally, thicker biofilms were usually healthier and stronger, although thickness was no guarantee for proper structure and power function as all factors were interdependent. There was an evolutionary trend that strong anodes became stronger/healthier and others weaker. This spontaneous trend has to be considered to avoid irreversible voltage reversals and to repair electrogenic biofilms in an MFC-Stack.

59 BASIC BIOLOGICAL SCIENCES↗
DOE OSTI2021

Metagenomic Insights Into the Microbial Iron Cycle of Subseafloor Habitats

Microbial iron cycling influences the flux of major nutrients in the environment (e.g., through the adsorptive capacity of iron oxides) and includes biotically induced iron oxidation and reduction processes. The ecological extent of microbial iron cycling is not well understood, even with increased sequencing efforts, in part due to limitations in gene annotation pipelines and limitations in experimental studies linking phenotype to genotype. This is particularly true for the marine subseafloor, which remains undersampled, but represents the largest contiguous habitat on Earth. To address this limitation, we used FeGenie, a database and bioinformatics tool that identifies microbial iron cycling genes and enables the development of testable hypotheses on the biogeochemical cycling of iron. Herein, we survey the microbial iron cycle in diverse subseafloor habitats, including sediment-buried crustal aquifers, as well as surficial and deep sediments. We inferred the genetic potential for iron redox cycling in 32 of the 46 metagenomes included in our analysis, demonstrating the prevalence of these activities across underexplored subseafloor ecosystems. We show that while some processes (e.g., iron uptake and storage, siderophore transport potential, and iron gene regulation) are near-universal, others (e.g., iron reduction/oxidation, siderophore synthesis, and magnetosome formation) are dependent on local redox and nutrient status. Additionally, we detected niche-specific differences in strategies used for dissimilatory iron reduction, suggesting that geochemical constraints likely play an important role in dictating the dominant mechanisms for iron cycling. Overall, our survey advances the known distribution, magnitude, and potential ecological impact of microbe-mediated iron cycling and utilization in sub-benthic ecosystems.

59 BASIC BIOLOGICAL SCIENCES↗
DOE OSTI2021

Silicate minerals as a direct source of limiting nutrients: Siderophore synthesis and uptake promote ferric iron bioavailability from olivine and microbial growth

Iron is a micronutrient critical to fundamental biological processes including respiration and photosynthesis, and it can therefore impact primary and heterotrophic productivity. Yet in oxic environments, iron is highly insoluble, rendering it, in principle, unavailable as a nutrient for biological growth. Life has “solved” this problem via the invention of iron chelates, known as siderophores, that keep iron available for microbial productivity. In this work, we examined the impact of siderophore synthesis on the speciation, mobility, and bioavailability of iron from rock-forming silicate minerals—shedding new light on the mechanisms by which microbes use mineral substrates to support primary productivity, as well as the consequent effects on silicate dissolution. Growth experiments were performed with Shewanella oneidensis MR-1 in an oxic, iron-depleted minimal medium, amended with olivine minerals as the sole source of iron. Experiments included the wild-type strain MR-1, and a siderophore synthesis gene deletion mutant strain (ΔMR-1). Relative to MR-1, ΔMR-1 exhibited a very pronounced growth penalty and an extended lag phase. However, substantial growth of ΔMR-1, comparable to MR-1 growth, was observed when the mutant strain was provided with siderophores in the form of either filtrate from a well-grown MR-1 culture, or commercially available deferoxamine. These observations suggest that siderophores are critical for S. oneidensis to acquire iron from olivine. Growth-limiting concentrations of deferoxamine amendments were observed to be ≤5–10 µM, concentrations significantly lower than previously recorded as necessary to impact mineral dissolution rates. X-ray photoelectric spectroscopy analyses of the incubated olivine surfaces suggest that siderophores deplete mineral surface layers of ferric iron. Combined, these results demonstrate that low micromolar concentrations of siderophores can effectively mobilize iron bound within silicate minerals, supporting very significant biological growth in limiting environments. The specific mechanism would involve siderophores removing a protective layer of nanometer-thick iron oxides, enhancing silicate dissolution and nutrient bioavailability.

59 BASIC BIOLOGICAL SCIENCES↗
DOE OSTI2021

Perseverance’s Scanning Habitable Environments with Raman and Luminescence for Organics and Chemicals (SHERLOC) Investigation

The Scanning Habitable Environments with Raman and Luminescence for Organics and Chemicals (SHERLOC) is a robotic arm-mounted instrument on NASA’s Perseverance rover. SHERLOC has two primary boresights. The Spectroscopy boresight generates spatially resolved chemical maps using fluorescence and Raman spectroscopy coupled to microscopic images (10.1 μm/pixel). The second boresight is a Wide Angle Topographic Sensor for Operations and eNgineering (WATSON); a copy of the Mars Science Laboratory (MSL) Mars Hand Lens Imager (MAHLI) that obtains color images from microscopic scales (~13 μm/pixel) to infinity. SHERLOC Spectroscopy focuses a 40 μs pulsed deep UV neon-copper laser (248.6 nm), to a ~100 μm spot on a target at a working distance of ~48 mm. Fluorescence emissions from organics, and Raman scattered photons from organics and minerals, are spectrally resolved with a single diffractive grating spectrograph with a spectral range of 250 to ~370 nm. Because the fluorescence and Raman regions are naturally separated with deep UV excitation (<250 nm), the Raman region ~ 800 – 4000 cm -1 (250 to 273 nm) and the fluorescence region (274 to ~370 nm) are acquired simultaneously without time gating or additional mechanisms. SHERLOC science begins by using an Autofocus Context Imager (ACI) to obtain target focus and acquire 10.1 μm/pixel greyscale images. Chemical maps of organic and mineral signatures are acquired by the orchestration of an internal scanning mirror that moves the focused laser spot across discrete points on the target surface where spectra are captured on the spectrometer detector. ACI images and chemical maps (< 100 μm/mapping pixel) will enable the first Mars in situ view of the spatial distribution and interaction between organics, minerals, and chemicals important to the assessment of potential biogenicity (containing CHNOPS). Single robotic arm placement chemical maps can cover areas up to 7x7 mm in area and, with the < 10 min acquisition time per map, larger mosaics are possible with arm movements. This microscopic view of the organic geochemistry of a target at the Perseverance field site, when combined with the other instruments, such as Mastcam-Z, PIXL, and SuperCam, will enable unprecedented analysis of geological materials for both scientific research and determination of which samples to collect and cache for Mars sample return.

46 INSTRUMENTATION RELATED TO NUCLEAR SCIENCE AND ↗
DOE OSTI2020

Single-Cell Genomics of Novel Actinobacteria With the Wood–Ljungdahl Pathway Discovered in a Serpentinizing System

Serpentinite-hosted systems represent modern-day analogs of early Earth environments. In these systems, water-rock interactions generate highly alkaline and reducing fluids that can contain hydrogen, methane, and low-molecular-weight hydrocarbons-potent reductants capable of fueling microbial metabolism. In this study, we investigated the microbiota of Hakuba Happo hot springs (~50°C; pH~10.5–11), located in Nagano (Japan), which are impacted by the serpentinization process. Analysis of the 16S rRNA gene amplicon sequences revealed that the bacterial community comprises Nitrospirae (47%), “Parcubacteria” (19%), Deinococcus-Thermus (16%), and Actinobacteria (9%), among others. Notably, only 57 amplicon sequence variants (ASV) were detected, and fifteen of these accounted for 90% of the amplicons. Among the abundant ASVs, an early-branching, uncultivated actinobacterial clade identified as RBG-16-55-12 in the SILVA database was detected. Ten single-cell genomes (average pairwise nucleotide identity: 0.98–1.00; estimated completeness: 33–93%; estimated genome size: ~2.3 Mb) that affiliated with this clade were obtained. Taxonomic classification using single copy genes indicates that the genomes belong to the actinobacterial class-level clade UBA1414 in the Genome Taxonomy Database. Based on metabolic pathway predictions, these actinobacteria are anaerobes, capable of glycolysis, dissimilatory nitrate reduction and CO 2 fixation via the Wood–Ljungdahl (WL) pathway. Several other genomes within UBA1414 and two related class-level clades also encode the WL pathway, which has not yet been reported for the Actinobacteria phylum. For the Hakuba actinobacterium, the energy metabolism related to the WL pathway is likely supported by a combination of the Rnf complex, group 3b and 3d [NiFe]-hydrogenases, [FeFe]-hydrogenases, and V-type (H + /Na + pump) ATPase. The genomes also harbor a form IV ribulose 1,5-bisphosphate carboxylase/oxygenase (RubisCO) complex, also known as a RubisCO-like protein, and contain signatures of interactions with viruses, including clustered regularly interspaced short palindromic repeat (CRISPR) regions and several phage integrases. This is the first report and detailed genome analysis of a bacterium within the Actinobacteria phylum capable of utilizing the WL pathway. The Hakuba actinobacterium is a member of the clade UBA1414/RBG-16-55-12, formerly within the group “OPB41.” We propose to name this bacterium ‘Candidatus Hakubanella thermoalkaliphilus.'

59 BASIC BIOLOGICAL SCIENCES↗
NASA NTRS2003

The NASA Astrobiology Roadmap

The NASA Astrobiology Roadmap provides guidance for research and technology development across the NASA enterprises that encompass the space, Earth, and biological sciences. The ongoing development of astrobiology roadmaps embodies the contributions of diverse scientists and technologists from government, universities, and private institutions. The Roadmap addresses three basic questions: How does life begin and evolve, does life exist elsewhere in the universe, and what is the future of life on Earth and beyond? Seven Science Goals outline the following key domains of investigation: understanding the nature and distribution of habitable environments in the universe, exploring for habitable environments and life in our own solar system, understanding the emergence of life, determining how early life on Earth interacted and evolved with its changing environment, understanding the evolutionary mechanisms and environmental limits of life, determining the principles that will shape life in the future, and recognizing signatures of life on other worlds and on early Earth. For each of these goals, Science Objectives outline more specific high-priority efforts for the next 3-5 years. These 18 objectives are being integrated with NASA strategic planning.

Exobiology/methods/trends↗
NASA NTRS2001

Mars Sample Handling Protocol Workshop Series

This report provides a record of the proceedings and recommendations of Workshop 3 of the Series, which was held in San Diego, California, March 19-21, 2001. Materials such as the Workshop agenda and participant lists as well as complete citations of all references and a glossary of terms and acronyms appear in the Appendices. Workshop 3 builds on the deliberations and findings of the earlier workshops in the Series, which have been reported separately. During Workshop 3, five individual sub-groups were formed to discuss the following topics: (1) Unifying Properties of Life, (2) Morphological organization and chemical properties, (3) Geochemical and geophysical properties, (4) Chemical Method and (5) Cell Biology Methods.

Race, Margaret S.↗
NASA NTRS2001

Organization of P, S, and Fe Inclusions in a Freshwater Magnetococcus

Magnetotactic bacteria are a heterogeneous group of motile, mainly aquatic procaryotes that align and swim along geomagnetic field lines. They are of interest to astrobiologists because of the magnetite crystals found in the Mars meteorite ALH84001 which share many characteristics with the magnetite produced intracellularly by magnetotactic bacteria. These bacteria are diverse morphologically, physiologically and phylogenetically, sharing a few key characteristics: 1) the presence of intracellular membrane-bound magnetic crystals (magnetosomes), usually but not always arranged in chains; 2) motility by means of flagella; and 3) microaerophillic or anaerobic physiology. The bilophotrichous (having two flagella bundles) magnetotactic cocci (MC) are ubiquitous in aquatic habitats but have proven extremely difficult to cultivate. Because only several marine strains have been isolated and grown in axenic culture, little is known about the physiology and the biogeochemical roles of the MC. We studied the composition and distribution of intracellular structures in an uncultured MC, designated ARB-1. To do this, a combination of light microscopy, environmental scanning electron microscopy (ESEM), transmission electron microscopy (TEM) and energy dispersive X-ray spectroscopy (EDS) were used. Cells of ARB-1 were separated from sediments collected from Baldwin Lake (Los Angeles Arboretum, Arcadia, CA). They are large spherical to oblate spheroidal Gram-negative cells, ranging from 1 to 4 micrometers along the maximum dimension, which is perpendicular to the direction of swimming. Cells have two large phosphorus-containing inclusions that comprise a large percentage of the cell volume. Many smaller sulfur inclusions are located at the convex end of the cell. Most of the cellular Fe is present in the magnetosomes. These may be arranged as a clump at the concave end of the cell, near the two flagella bundles, or as chains, or as both a clump and chains. The magnetosomes were identified as magnetite (Fe3O4) by selected area electron diffraction (SAED) and high resolution TEM. We saw a trend between cell size and organization of the magnetosomes. Smaller, more spherical cells were more likely to have chains than were larger, more oblate cells. This may indicate different populations of cells, or it may be attributed to variations in cell growth cycle. The size distribution (length) of magnetosomes in chains was similar to that of magnetosomes in clusters, except that there was a larger size range for clustered magnetosomes. Magnetosomes from ARB-1 cells average 82 nm in length. If plotted on a graph of length as a function of aspect ratio, they fall within the single domain region of the plot. If compared with the size distributions of magnetite from ALH84001 and magnetosomes from the cultured magnetotactic vibrio MV-1, the magnetites produced by ARB-1 cells are, on average, larger and have a wider range of aspect ratio. ARB-1 cells have a specific organization of the P, S, and Fe inclusions. The P inclusions always occupy the majority of the cell volume and separate the S inclusions from the disorganized clumps of magnetosomes and the flagella bundles. The P inclusions may contain polyphosphate, which could play several roles in motility, adaptation to stress, growth and division, buoyancy, and energy. The S inclusions might be a way to store S, a potential energy source, when the cells move from sulfide to oxygen zones. The consistency of P, S, and Fe organization in ARB-1 cells suggests that these inclusions have some specific and interactive functions.

Cox, Lea↗
NASA NTRS2001

The Fe-Isotope System and Its Applicability as a Biosignature

High precision (0.05) Fe isotope analyses show that igneous rocks and loess are invariant but chemical sediments have variable compositions. The relative roles of abiologic and biologic fractionations that produced this range are discussed. Additional information is contained in the original extended abstract.

Beard, Brian L.↗
NASA NTRS1999

Mars Sample Handling and Requirements Panel (MSHARP)

In anticipation of the return of samples from Mars toward the end of the first decade of the next century, NASA's Office of Space Sciences chartered a panel to examine how Mars samples should be handled. The panel was to make recommendations in three areas: (1) sample collection and transport back to Earth; (2) certification of the samples as nonhazardous; and (3) sample receiving, curation, and distribution. This report summarizes the findings of that panel. The samples should be treated as hazardous until proven otherwise. They are to be sealed within a canister on Mars, and the canister is not to be opened until within a Biosafety Hazard Level 4 (BSL-4) containment facility here on Earth. This facility must also meet or exceed the cleanliness requirements of the Johnson Space Center (JSC) facility for curation of extraterrestrial materials. A containment facility meeting both these requirements does not yet exist. Hazard assessment and life detection experiments are to be done at the containment facility, while geochemical characterization is being performed on a sterilized subset of the samples released to the science community. When and if the samples are proven harmless, they are to be transferred to a curation facility, such as that at JSC.

Carr, Michael H.↗
NASA NTRS1993

Planetary Biology and Microbial Ecology: Molecular Ecology and the Global Nitrogen cycle

This report summarizes the results of the Planetary Biology and Molecular Ecology's summer 1991 program, which was held at the Marine Biological Laboratory in Woods Hole, Massachusetts. The purpose of the interdisciplinary PBME program is to integrate, via lectures and laboratory work, the contributions of university and NASA scientists and student interns. The goals of the 1991 program were to examine several aspects of the biogeochemistry of the nitrogen cycle and to teach the application of modern methods of molecular genetics to field studies of organisms. Descriptions of the laboratory projects and protocols and abstracts and references of the lectures are presented.

Nealson, Molly Stone↗
NASA NTRS1990

The biogeochemistry of metal cycling

The results of the Planetary Biology and Microbial Ecology's summer 1987 program are summarized. The purpose of the interdisciplinary PBME program is to integrate, via lectures and laboratory work, the contributions of university and NASA scientists and student interns. The 1987 program examined various aspects of the biogeochemistry of metal cycling, and included such areas as limnology, metal chemistry, metal geochemistry, microbial ecology, and interactions with metals. A particular area of focus was the use of remote sensing in the study of biogeochemistry. Abstracts and bibliographies of the lectures and reports of the laboratory projects are presented.

Nealson, Kenneth H.↗
NASA NTRS1989

Distributions of Manganese, Iron, and Manganese-Oxidizing Bacteria In Lake Superior Sediments of Different Organic Carbon Content

Profiles of oxygen, soluble and particulate manganese and iron, organic carbon and nitrogen were examined in Lake Superior sediment cores, along with the distribution and abundance of heterotrophic and manganese oxidizing bacteria. Analyses were performed using cores collected with the submersible Johnson Sea Link II. Three cores, exhibiting a range of organic carbon content, were collected from the deepest basin in Lake Superior and the north and south ends of the Caribou trough, and brought to the surface for immediate analysis. Minielectrode profiles of oxygen concentration of the three cores were carried out using a commercially available minielectrode apparatus. Oxygen depletion to less than 1% occurred within 4 cm of the surface for two of the cores, but not until approximately 15 cm for the core from the south basin of the Caribou trough. The three cores exhibited very different profiles of soluble, as well as leachable, manganese and iron, suggesting different degrees of remobilization of these metals in the sediments. Vertical profiles of viable bacteria and Mn oxidizing bacteria, determined by plating and counting, showed that aerobic (and facultatively aerobic) heterotrophic bacteria were present at the highest concentrations near the surface and decreased steadily with depth, while Mn oxidizing bacteria were concentrations primarily at and above the oxic/anoxic interface. Soluble manganese in the pore waters, along with abundant organic carbon, appeared to enhance the presence of manganese oxidizing bacteria, even below the oxic/anoxic interface. Profiles of solid-phase leachable manganese suggested a microbial role in manganese reprecipitation in these sediments.

Richardson, Laurie L.↗
NASA NTRS1988

Microbial reduction of manganese oxides - Interactions with iron and sulfur

Alteromonas putrefaciens (strain MR-1) is capable of rapid Mn(IV) reduction under conditions of neutral pH and temperatures characteristic of the Oneida Lake, New York, sediments from which it was isolated. MR-1 also reduces Fe(3+) to Fe(2+), and disproportionates thiosulfate to sulfide and sulfite; independently, the Fe(2+) and sulfide act as rapid reductants of Mn. The addition of Fe(3+) or thiosulfate to cultures of MR-1 in the presence of oxidized Mn increases the rate and the extent of Mn reduction relative to that observed in the absence of Fe(3+) or thiosulfate. Furthermore, when Fe(3+) and Mn oxides are present conjointly, Fe(2+) does not appear until the reduction of the oxidized Mn is complete. These results demonstrate that the observed rates of Fe(2+) and sulfide production may underestimate the total rates of Fe and sulfate reduction in those environments containing oxidized Mn. These results also demonstrate the potential impact that a single microbe can exert on sediment geochemistry, and provide the basis for preliminary models of the complexity of microbial and geochemical interactions that occur.

Myers, Charles R.↗
NASA NTRS1988

Bacterial manganese reduction and growth with manganese oxide as the sole electron acceptor

Microbes that couple growth to the reduction of manganese could play an important role in the biogeochemistry of certain anaerobic environments. Such a bacterium, Alteromonas putrefaciens MR-1, couples its growth to the reduction of manganese oxides only under anaerobic conditions. The characteristics of this reduction are consistent with a biological, and not an indirect chemical, reduction of manganese, which suggest that this bacterium uses manganic oxide as a terminal electron acceptor. It can also utilize a large number of other compounds as terminal electron acceptors; this versatility could provide a distinct advantage in environments where electron-acceptor concentrations may vary.

Myers, Charles R.↗