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Search indexed NASA NTRS and DOE OSTI research on propulsion, heat transfer, battery materials and energy systems. Follow report and document links to the original sources.

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16 records
All sourcesNASA NTRSDOE OSTI
NASA NTRS2004

A genomic timescale of prokaryote evolution: insights into the origin of methanogenesis, phototrophy, and the colonization of land

BACKGROUND: The timescale of prokaryote evolution has been difficult to reconstruct because of a limited fossil record and complexities associated with molecular clocks and deep divergences. However, the relatively large number of genome sequences currently available has provided a better opportunity to control for potential biases such as horizontal gene transfer and rate differences among lineages. We assembled a data set of sequences from 32 proteins (approximately 7600 amino acids) common to 72 species and estimated phylogenetic relationships and divergence times with a local clock method. RESULTS: Our phylogenetic results support most of the currently recognized higher-level groupings of prokaryotes. Of particular interest is a well-supported group of three major lineages of eubacteria (Actinobacteria, Deinococcus, and Cyanobacteria) that we call Terrabacteria and associate with an early colonization of land. Divergence time estimates for the major groups of eubacteria are between 2.5-3.2 billion years ago (Ga) while those for archaebacteria are mostly between 3.1-4.1 Ga. The time estimates suggest a Hadean origin of life (prior to 4.1 Ga), an early origin of methanogenesis (3.8-4.1 Ga), an origin of anaerobic methanotrophy after 3.1 Ga, an origin of phototrophy prior to 3.2 Ga, an early colonization of land 2.8-3.1 Ga, and an origin of aerobic methanotrophy 2.5-2.8 Ga. CONCLUSIONS: Our early time estimates for methanogenesis support the consideration of methane, in addition to carbon dioxide, as a greenhouse gas responsible for the early warming of the Earths' surface. Our divergence times for the origin of anaerobic methanotrophy are compatible with highly depleted carbon isotopic values found in rocks dated 2.8-2.6 Ga. An early origin of phototrophy is consistent with the earliest bacterial mats and structures identified as stromatolites, but a 2.6 Ga origin of cyanobacteria suggests that those Archean structures, if biologically produced, were made by anoxygenic photosynthesizers. The resistance to desiccation of Terrabacteria and their elaboration of photoprotective compounds suggests that the common ancestor of this group inhabited land. If true, then oxygenic photosynthesis may owe its origin to terrestrial adaptations.

Methane/metabolism↗
DOE OSTI2022

Phototrophy and carbon fixation in Chlorobi postdate the rise of oxygen

While most productivity on the surface of the Earth today is fueled by oxygenic photosynthesis, for much of Earth history it is thought that anoxygenic photosynthesis—using compounds like ferrous iron or sulfide as electron donors—drove most global carbon fixation. Anoxygenic photosynthesis is still performed by diverse bacteria in niche environments today. Of these, the Chlorobi (formerly green sulfur bacteria) are often interpreted as being particularly ancient and are frequently proposed to have fueled the biosphere during late Archean and early Paleoproterozoic time before the rise of oxygenic photosynthesis. Here, we perform comparative genomic, phylogenetic, and molecular clock analyses to determine the antiquity of the Chlorobi and their characteristic phenotypes. We show that contrary to common assumptions, the Chlorobi clade is relatively young, with anoxygenic phototrophy, carbon fixation via the rTCA pathway, and iron oxidation all significantly postdating the rise of oxygen ~2.3 billion years ago. The Chlorobi therefore could not have fueled the Archean biosphere, but instead represent a relatively young radiation of organisms which likely acquired the capacity for anoxygenic photosynthesis and other traits via horizontal gene transfer sometime after the evolution of oxygenic Cyanobacteria.

59 BASIC BIOLOGICAL SCIENCES↗
DOE OSTI2024

Anoxygenic phototroph of the Chloroflexota uses a type I reaction centre

Scientific exploration of phototrophic bacteria over nearly 200 years has revealed large phylogenetic gaps between known phototrophic groups that limit understanding of how phototrophy evolved and diversified. Here, through Boreal Shield lake water incubations, we cultivated an anoxygenic phototrophic bacterium from a previously unknown order within the Chloroflexota phylum that represents a highly novel transition form in the evolution of photosynthesis. Unlike all other known phototrophs, this bacterium uses a type I reaction centre (RCI) for light energy conversion yet belongs to the same bacterial phylum as organisms that use a type II reaction centre (RCII) for phototrophy. Using physiological, phylogenomic and environmental metatranscriptomic data, we demonstrate active RCI-utilizing metabolism by the strain alongside usage of chlorosomes and bacteriochlorophylls related to those of RCII-utilizing Chloroflexota members. Despite using different reaction centres, our phylogenomic data provide strong evidence that RCI-utilizing and RCII-utilizing Chloroflexia members inherited phototrophy from a most recent common phototrophic ancestor. The Chloroflexota phylum preserves an evolutionary record of the use of contrasting phototrophic modes among genetically related bacteria, giving new context for exploring the diversification of phototrophy on Earth.

59 BASIC BIOLOGICAL SCIENCES↗
DOE OSTI2021

Deletion of the cytochrome bc complex from Heliobacterium modesticaldum results in viable but non-phototrophic cells

The heliobacteria, a family of anoxygenic phototrophs, possess the simplest known photosynthetic apparatus. Although they are photoheterotrophs in the light, the heliobacteria can also grow chemotrophically via pyruvate metabolism in the dark. In the heliobacteria, the cytochrome bc complex is responsible for oxidizing menaquinol and reducing cytochrome c 553 in the electron flow cycle used for phototrophy. However, there is no known electron acceptor for the mobile cytochrome c 553 other than the photochemical reaction center. We have, therefore, hypothesized that the cytochrome bc complex is necessary for phototrophy, but unnecessary for chemotrophic growth in the dark. Here, we used a two-step method for CRISPR-based genome editing in Heliobacterium modesticaldum to delete the genes encoding the four major subunits of the cytochrome bc complex. Genotypic analysis verified the deletion of the petCBDA gene cluster encoding the catalytic components of the complex. Spectroscopic studies revealed that re-reduction of cytochrome c 553 after flash-induced photo-oxidation was over 100 times slower in the petCBDA mutant compared to the wild-type. Steady-state levels of oxidized P 800 (the primary donor of the photochemical reaction center) were much higher in the petCBDA mutant at every light level, consistent with a limitation in electron flow to the reaction center. The petCBDA mutant was unable to grow phototrophically on acetate plus CO 2 but could grow chemotrophically on pyruvate as a carbon source similar to the wild-type strain in the dark. The mutants could be complemented by reintroduction of the petCBDA gene cluster on a plasmid expressed from the clostridial eno promoter.

59 BASIC BIOLOGICAL SCIENCES↗
DOE OSTI2023

Mixotrophic microbes create carbon tipping points under warming

Mixotrophs are ubiquitous and integral to microbial food webs, but their impacts on the dynamics and functioning of broader ecosystems are largely unresolved. Here, we show that mixotrophy produces a unique type of food web module that exhibits unusual ecological dynamics, with surprising consequences for carbon flux under warming. We develop a generalizable model of a mixotrophic food web module that incorporates dynamic switching between phototrophy and phagotrophy to assess ecological dynamics and total system CO 2 flux. We find that warming switches mixotrophic systems between alternative stable carbon states—including a phototrophy-dominant carbon sink state, a phagotrophy-dominant carbon source state and cycling between these two. Moreover, warming always shifts this mixotrophic system from a carbon sink state to a carbon source state, but a coordinated increase in nutrients can erase early warning signals of this transition and expand hysteresis. This suggests that mixotrophs can generate critical carbon tipping points under warming that will be more abrupt and less reversible when combined with increased nutrient levels, having widespread implications for ecosystem functioning in the face of rapid global change.

54 ENVIRONMENTAL SCIENCES↗
DOE OSTI2021

Granick revisited: Synthesizing evolutionary and ecological evidence for the late origin of bacteriochlorophyll via ghost lineages and horizontal gene transfer

Photosynthesis—both oxygenic and more ancient anoxygenic forms—has fueled the bulk of primary productivity on Earth since it first evolved more than 3.4 billion years ago. However, the early evolutionary history of photosynthesis has been challenging to interpret due to the sparse, scattered distribution of metabolic pathways associated with photosynthesis, long timescales of evolution, and poor sampling of the true environmental diversity of photosynthetic bacteria. Here, we reconsider longstanding hypotheses for the evolutionary history of phototrophy by leveraging recent advances in metagenomic sequencing and phylogenetics to analyze relationships among phototrophic organisms and components of their photosynthesis pathways, including reaction centers and individual proteins and complexes involved in the multi-step synthesis of (bacterio)-chlorophyll pigments. We demonstrate that components of the photosynthetic apparatus have undergone extensive, independent histories of horizontal gene transfer. This suggests an evolutionary mode by which modular components of phototrophy are exchanged between diverse taxa in a piecemeal process that has led to biochemical innovation. We hypothesize that the evolution of extant anoxygenic photosynthetic bacteria has been spurred by ecological competition and restricted niches following the evolution of oxygenic Cyanobacteria and the accumulation of O 2 in the atmosphere, leading to the relatively late evolution of bacteriochlorophyll pigments and the radiation of diverse crown group anoxygenic phototrophs. This hypothesis expands on the classic “Granick hypothesis” for the stepwise evolution of biochemical pathways, synthesizing recent expansion in our understanding of the diversity of phototrophic organisms as well as their evolving ecological context through Earth history.

58 GEOSCIENCES↗
DOE OSTI2021

Single-cell visualization and quantification of trace metals in Chlamydomonas lysosome-related organelles

Significance Transition metals are of crucial importance for primary productivity; their scarcity limits crop yield in agriculture and carbon sequestration on a global scale. Copper (Cu), iron (Fe), and manganese (Mn) are among the most important trace elements that enable the redox chemistry in oxygenic photosynthesis. The single-celled, eukaryotic green alga Chlamydomonas reinhardtii is a choice experimental system for studying trace metal homeostasis in the context of phototrophy, offering all the advantages of a classical microbial system with a well-characterized photosystem and trace metal metabolism machinery of relevance to plants. This project identifies and differentiates different trace metal storage sites in Chlamydomonas and uncovers the dynamics of trace metal storage and mobilization in situations of fluctuating resources.

54 ENVIRONMENTAL SCIENCES↗
DOE OSTI2020

Ecological and genomic analyses of candidate phylum WPS-2 bacteria in an unvegetated soil

Members of the bacterial candidate phylum WPS-2 (or Eremiobacterota) are abundant in several dry, bare soil environments. In a bare soil deposited by an extinct iron-sulfur spring, we found that WPS-2 comprised up to 24% of the bacterial community and up to 108 cells per g of soil based on 16S rRNA gene sequencing and quantification. A single genus-level cluster (Ca. Rubrimentiphilum) predominated in bare soils but was less abundant in adjacent forest. Nearly complete genomes of Ca. Rubrimentiphilum were recovered as single amplified genomes (SAGs) and metagenome-assembled genomes (MAGs). Surprisingly, given the abundance of WPS-2 in bare soils, the genomes did not indicate any capacity for autotrophy, phototrophy, or trace gas metabolism. Instead, they suggest a predominantly aerobic organoheterotrophic lifestyle, perhaps based on scavenging amino acids, nucleotides, and complex oligopeptides, along with lithotrophic capacity on thiosulfate. Network analyses of the entire community showed that some species of Chloroflexi, Actinobacteria, and candidate phylum AD3 (or Dormibacterota) co-occurred with Ca. Rubrimentiphilum and may represent ecological or metabolic partners. We propose that Ca. Rubrimentiphilum act as efficient heterotrophic scavengers. Combined with previous studies, these data suggest that the phylum WPS-2 includes bacteria with diverse metabolic capabilities.

59 BASIC BIOLOGICAL SCIENCES↗
DOE OSTI2025

Cryptic cycling by electroactive bacterioplankton in Trout Bog Lake

The potential for extracellular electron transfer (EET) is a prevailing genomic feature of humic lake bacterioplankton. However, there has been little evidence for the substantial ecological contribution predicted by genetics. We hypothesized that anoxygenic phototrophic electrotrophs and accompanying heterotrophic electrogens cycle dissolved organic matter (DOM) between oxidized and reduced states. We predicted that such bacterioplankton would exhibit diel-scale oscillations due to the light dependency of photosynthesis. Using Trout Bog Lake in Wisconsin, USA, as our model ecosystem, we profiled the water column with depth-discrete metagenomic, physiochemical, and electrochemical analyses. We observed variation in oxidation reduction potential (ORP) in response to sunlight, initiating at depths populated by anoxygenic phototrophs with EET genes. We developed an automated buoy to measure electric current flow between many pairs of electrodes simultaneously, observing correlation in electron consumption to sunlight. Our results, combined with published metatranscriptomic analysis, indicate the occurrence of electron cycling between phototrophic oxidation (electrotrophic metabolism) by Chlorobium and anaerobic respiration (electrogenic metabolism) by Geothrix, involving DOM. We also repeatedly observed gradual seasonal increases in hypolimnion ORP throughout summer. These diel and seasonal patterns imply that electroactive DOM mediates the ecology of electroactive bacteria in lakes, controlling humic lake methane emissions.IMPORTANCEWe investigated the physical, chemical, and redox characteristics of a bog lake and electrodes hung therein to test the hypothesis that dissolved organic matter is being cycled between oxidized and reduced states by electroactive bacterioplankton powered by phototrophy. To do so, we performed field-based analyses on multiple timescales using both established and novel instrumentation. We paired these analyses with recently developed bioinformatics pipelines for metagenomics data to investigate genes that enable electroactive metabolism and accompanying metabolisms. Our results are consistent with our hypothesis and yet upend some of our other expectations. Our findings have implications for understanding greenhouse gas emissions from lakes, including electroactivity as an integral part of lake metabolism throughout more of the anoxic parts of lakes and for a longer portion of the summer than expected. Our results also give a sense of what electroactivity occurs at given depths and provide a strong basis for future studies.

carbon emissions↗
DOE OSTI2024

Using a systems biology approach to describe the role of dissimilatory phosphite oxidation in the global phosphorus cycle

We investigated the role of redox reactions in the global phosphorous (P) cycle. We identified novel microbial processes responsible for oxidation of reduced phosphorous in the form of phosphite producing bioavailable phosphate. We identified central tenets that define microbial dissimilatory phosphite oxidation (DPO) and the breadth of the taxonomy of DPO microorganisms (DPOM). We demonstrated that this metabolism is vertically evolved from 3.8 GYA contemporaneously with anoxygenic phototrophy. We further demonstrate its occurrence on extant Earth as a primary mechanism driving a phosphorous redox cycle. Finally, we showed that this metabolism is environmentally maintained by the newly described autotrophic Phosphitivorax genus which rely on the reductive glycine pathway for carbon fixation. Our results demonstrate that these species are involved in a complex nutrient-dependent symbiotic relationship with their community in which they provide the fixed carbon to support the heterotrophic community and in return receive prerequisite corrinoids to maintain their activities.

54 ENVIRONMENTAL SCIENCES↗
DOE OSTI2021

Genomic and Phenotypic Characterization of Chloracidobacterium Isolates Provides Evidence for Multiple Species

Chloracidobacterium is the first and until now the sole genus in the phylum Acidobacteriota (formerly Acidobacteria ) whose members perform chlorophyll-dependent phototrophy (i.e., chlorophototrophy). An axenic isolate of Chloracidobacterium thermophilum (strain B T ) was previously obtained by using the inferred genome sequence from an enrichment culture and diel metatranscriptomic profiling analyses in situ to direct adjustments to the growth medium and incubation conditions, and thereby a defined growth medium for Chloracidobacterium thermophilum was developed. These advances allowed eight additional strains of Chloracidobacterium spp. to be isolated from microbial mat samples collected from Mushroom Spring, Yellowstone National Park, United States, at temperatures of 41, 52, and 60°C; an axenic strain was also isolated from Rupite hot spring in Bulgaria. All isolates are obligately photoheterotrophic, microaerophilic, non-motile, thermophilic, rod-shaped bacteria. Chloracidobacterium spp. synthesize multiple types of (bacterio-)chlorophylls and have type-1 reaction centers like those of green sulfur bacteria. Light harvesting is accomplished by the bacteriochlorophyll a -binding, Fenna-Matthews-Olson protein and chlorosomes containing bacteriochlorophyll c . Their genomes are approximately 3.7 Mbp in size and comprise two circular chromosomes with sizes of approximately 2.7 Mbp and 1.0 Mbp. Comparative genomic studies and phenotypic properties indicate that the nine isolates represent three species within the genus Chloracidobacterium . In addition to C. thermophilum , the microbial mats at Mushroom Spring contain a second species, tentatively named Chloracidobacterium aggregatum , which grows as aggregates in liquid cultures. The Bulgarian isolate, tentatively named Chloracidobacterium validum , will be proposed as the type species of the genus, Chloracidobacterium. Additionally, Chloracidobacterium will be proposed as the type genus of a new family, Chloracidobacteriaceae , within the order Blastocatellales , the class Blastocatellia , and the phylum Acidobacteriota.

59 BASIC BIOLOGICAL SCIENCES↗
NASA NTRS2005

Aerobic Anoxygenic Phototrophic Bacteria in the Mid-Atlantic Bight and the North Pacific Gyre

The abundance of aerobic anoxygenic phototrophic (AM) bacteria, cyanobacteria and heterotrophs was examined in the Mid-Atlantic Bight and the central North Pacific gyre using infrared fluorescence microscopy coupled with image analysis and flow cytometry. AAP bacteria comprised 5% to 16% of total prokaryotes in the Atlantic but only 5% or less in the Pacific. In the Atlantic, AAP bacterial abundance was as much as 2-fold higher than Prochlorococcus and 10-folder higher than Synechococcus. In contrast, Prochlorococcus outnumbered AAP bacteria 5- to 50-fold in the Pacific. In both oceans, subsurface abundance maxima occurred within the photic zone, and AAP bacteria were least abundant below the 1% light depth. Concentrations of bacteriochlorophyll a (BChl a) were low (approx.1%) compared to chlorophyll a. Although the BChl a content of AAP bacteria per cell was typically 20- to 250-fold lower than the divinyl-chlorophyll a content of Prochlorococcus, in shelf break water the pigment content of AAP bacteria approached that of Prochlorococcus. The abundance of AAP bacteria rivaled some groups of strictly heterotrophic bacteria and was often higher than the abundance of known AAP genera (Erythrobacter and Roseobacter spp.). The distribution of AAP bacteria in the water column, which was similar in the Atlantic and the Pacific, was consistent with phototrophy.

Cottrell, Matthew T.↗
NASA NTRS2012

Photosystem Trap Energies and Spectrally-Dependent Energy-Storage Efficiencies in the Chl d-Utilizing Cyanobacterium, Acaryochloris Marina

Acaryochloris marina is the only species known to utilize chlorophyll (Chl) d as a principal photopigment. The peak absorption wavelength of Chl d is redshifted approx. 40 nm in vivo relative to Chl a, enabling this cyanobacterium to perform oxygenic phototrophy in niche environments enhanced in far-red light. We present measurements of the in vivo energy-storage (E-S) efficiency of photosynthesis in A. marina, obtained using pulsed photoacoustics (PA) over a 90-nm range of excitation wavelengths in the red and far-red. Together with modeling results, these measurements provide the first direct observation of the trap energies of PSI and PSII, and also the photosystem-specific contributions to the total E-S efficiency. We find the maximum observed efficiency in A. marina (40+/-1% at 735 nm) is higher than in the Chl a cyanobacterium Synechococcus leopoliensis (35+/-1% at 690 nm). The efficiency at peak absorption wavelength is also higher in A. marina (36+/-1% at 710 nm vs. 31+/-1% at 670 nm). In both species, the trap efficiencies are approx. 40% (PSI) and approx. 30% (PSII). The PSI trap in A. marina is found to lie at 740+/-5 nm, in agreement with the value inferred from spectroscopic methods. The best fit of the model to the PA data identifies the PSII trap at 723+/-3 nm, supporting the view that the primary electron-donor is Chl d, probably at the accessory (ChlD1) site. A decrease in efficiency beyond the trap wavelength, consistent with uphill energy transfer, is clearly observed and fit by the model. These results demonstrate that the E-S efficiency in A. marina is not thermodynamically limited, suggesting that oxygenic photosynthesis is viable in even redder light environments.

Mielke, Steven P.↗
DOE OSTI2021

Photosynthesis | The Heliobacteria

The heliobacteria are the only phototrophs in the Gram-positive group of bacteria. They are strict anaerobes that grow in a primarily fermentative mode in the dark. In the light, they use a homodimeric Type I photochemical reaction center to drive cyclic electron transport. They are unique in using the pigment bacteriochlorophyll g. All heliobacteria are unable to fix CO 2 but able to fix N2. Their core metabolism includes a complete TCA cycle with several reversible enzymes in common with the reverse (reductive) TCA cycle, but they lack an (ATP) citrate lyase that would allow CO 2 fixation. There are now several sequenced genomes available for different heliobacterial species, allowing hypotheses to be made concerning their metabolic potential. Here, techniques to introduce replicating plasmids into Heliobacterium modesticaldum, as well as leveraging its endogenous CRISPR/Cas system to edit its chromosome, have recently been pioneered, contributing to making this species a model system for this family.

59 BASIC BIOLOGICAL SCIENCES↗
DOE OSTI2020

Microbial community dynamics and coexistence in a sulfide-driven phototrophic bloom

Background: Lagoons are common along coastlines worldwide and are important for biogeochemical element cycling, coastal biodiversity, coastal erosion protection and blue carbon sequestration. These ecosystems are frequently disturbed by weather, tides, and human activities. Here, we investigated a shallow lagoon in New England. The brackish ecosystem releases hydrogen sulfide particularly upon physical disturbance, causing blooms of anoxygenic sulfur-oxidizing phototrophs. To study the habitat, microbial community structure, assembly and function we carried out in situ experiments investigating the bloom dynamics over time. Results: Phototrophic microbial mats and permanently or seasonally stratified water columns commonly contain multiple phototrophic lineages that coexist based on their light, oxygen and nutrient preferences. We describe similar coexistence patterns and ecological niches in estuarine planktonic blooms of phototrophs. The water column showed steep gradients of oxygen, pH, sulfate, sulfide, and salinity. The upper part of the bloom was dominated by aerobic phototrophic Cyanobacteria, the middle and lower parts by anoxygenic purple sulfur bacteria (Chromatiales) and green sulfur bacteria (Chlorobiales), respectively. We show stable coexistence of phototrophic lineages from five bacterial phyla and present metagenome-assembled genomes (MAGs) of two uncultured Chlorobaculum and Prosthecochloris species. In addition to genes involved in sulfur oxidation and photopigment biosynthesis the MAGs contained complete operons encoding for terminal oxidases. The metagenomes also contained numerous contigs affiliating with Microviridae viruses, potentially affecting Chlorobi. Our data suggest a short sulfur cycle within the bloom in which elemental sulfur produced by sulfide-oxidizing phototrophs is most likely reduced back to sulfide by Desulfuromonas sp. Conclusions: The release of sulfide creates a habitat selecting for anoxygenic sulfur-oxidizing phototrophs, which in turn create a niche for sulfur reducers. Strong syntrophism between these guilds apparently drives a short sulfur cycle that may explain the rapid development of the bloom. The fast growth and high biomass yield of Chlorobi-affiliated organisms implies that the studied lineages of green sulfur bacteria can thrive in hypoxic habitats. This oxygen tolerance is corroborated by oxidases found in MAGs of uncultured Chlorobi. The findings improve our understanding of the ecology and ecophysiology of anoxygenic phototrophs and their impact on the coupled biogeochemical cycles of sulfur and carbon.

59 BASIC BIOLOGICAL SCIENCES↗