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NASA NTRS1989

Biological nitrogen fixation under primordial Martian partial pressures of dinitrogen

One of the most striking differences between the conditions on early Mars and earth was a low (18 mb) partial pressure of N2 (pN2) on early Mars, as opposed to 780 mb N2 on earth. To investigate the possibility of biological nitrogen fixation under conditions of early Mars, experiments were carried out on the growth of Azotobacter vinelandii and Azomonas agilis in nitrogen-free synthetic medium under various partial pressures of N2 (ranging from 780 to 0 mb). It was found that, although the biomass, cell number, and growth rate of these bacteria decreased with decreasing pN2 values below pN2 of 400 mb, both microorganisms were capable of growing at pN2 as low as 5 mb (but not at of below 1 mb), indicating that biological fixation of nitrogen could have occurred on primordial Mars.

Klingler, J. M.↗

NASA NTRS2012

Microgravity Effects on the Early Events of Biological Nitrogen Fixation in Medicago Truncatula: Results from the SyNRGE Experiment

Stutte, Gary W.↗

NASA NTRS2011

Effect of Microgravity on Early Events of Biological Nitrogen Fixation in Medicago Truncatula: Initial Results from the SyNRGE Experiment

SyNRGE (Symbiotic Nodulation in a Reduced Gravity Environment) was a sortie mission on STS-135 in the Biological Research in Canisters (BRIC) hardware to study the effect of microgravity on a plant-microbe symbiosis resulting in biological nitrogen fixation. Medicago truncatula, a model species of the legume family, was inoculated with its bacterial symbiont, Sinorhizobium meliloti, to observe early events associated with infection and nodulation in Petri Dish Fixation Units (PDFUs). Two sets of experiments were conducted in orbit and in 24-hour delayed ground controls. Experiment one was designed to determine if S. meliloti infect M. truncatula and initiate physiological changes associated with nodule formation. Roots of five-day-old M. truncatula cultivar Jemalong A17 (Enodll::gus) were inoculated 24 hr before launch with either S. meliloti strain 1021 or strain ABS7 and integrated into BRIC-PDFU hardware placed in a 4 C Cold Bag for launch on Atlantis. Inoculated plants and uninoculated controls were maintained in the dark at ambient temperature in the middeck of STS-135 for 11 days before fixation in RNAlater(tM) by crew activation of the PDFU. Experiment two was designed to determine if microgravity altered the process of bacterial infection and host plant nodule formation. Seeds of two M. truncatula cultivar Jemalong A17 lines, the Enodll::gus used in experiment 1, and SUNN, a super-nodulating mutant of A17, were germinated on orbit for 11 days in the middeck cabin and returned to Earth alive inside of BRIC-PDFU's at 4 C. S. meliloti strains 1021 and ABS7 were cultivated separately in broth culture on orbit and also returned to Earth alive. After landing, flight- and groundgrown plants and bacteria were transferred from BRIC-PDFU's into Nunc(tm) 4-well plates for reciprocity crosses. Rates of plant growth and nodule development on Buffered Nodulation Medium (lacking nitrogen) were measured for 14 days. Preliminary analysis' of Experiment 1 confirms that legumes and bacteria cultivated in space 'initiate the symbiotic interaction leading to nitrogen fixation and that bacteria retain the ability to form nodules on M. truncatula roots. Initial assessment of experiment 2 shows 100% seed germination and excellent bacterial growth in microgravity.

Stutte, Gary W.↗

NASA NTRS1988

The evolution of nitrogen cycling

The energetics of nitrogen transformation reactions and the evolution of nitrogen cycling are examined. It is suggested that meteor impact-produced fixed nitrogen could have caused the entire reservoir of the earth's N2 to convert into fixed nitrogen at the end of accretion. The abiotic fixation rate on the early earth by lightning is estimated at about 1-3 X 10 to the 16th molecules of NO/J. It is found that biological nitrogen fixation may have evolved after the development of an aerobic atmosphere. It is shown that HNO could eventually become NO2(-) and NO3(-) after reaching the earth's surface. It is concluded that the evolutionary sequence for the biological transformation of nitrogen compounds is ammonification - denitrification - nitrification - nitrogen fixation.

Mancinelli, Rocco L.↗

NASA NTRS2023

Regulatory response to a hybrid ancestral nitrogenase in Azotobacter vinelandii

Biological nitrogen fixation, the microbial reduction of atmospheric nitrogen to bioavailable ammonia, represents both a major limitation on biological productivity and a highly desirable engineering target for synthetic biology. However, the engineering of nitrogen fixation requires an integrated understanding of how the gene regulatory dynamics of host diazotrophs respond across sequence-function space of its central catalytic metalloenzyme, nitrogenase. Here, we interrogate this relationship by analyzing the transcriptome of Azotobacter vinelandii engineered with a phylogenetically inferred ancestral nitrogenase protein variant. The engineered strain exhibits reduced cellular nitrogenase activity but recovers wild-type growth rates following an extended lag period. We find that expression of genes within the immediate nitrogen fixation network is resilient to the introduced nitrogenase sequence-level perturbations. Rather the sustained physiological compatibility with the ancestral nitrogenase variant is accompanied by reduced expression of genes that support trace metal and electron resource allocation to nitrogenase. Our results spotlight gene expression changes in cellular processes adjacent to nitrogen fixation as productive engineering considerations to improve compatibility between remodeled nitrogenase proteins and engineered host diazotrophs.

nitrogen fixation↗

NASA NTRS1989

Life sciences and space research XXIII(2): Planetary biology and origins of life; Proceedings of the Topical Meeting and Workshops XX, XXI and XXIII of the 27th COSPAR Plenary Meeting, Espoo, Finland, July 18-29, 1988

This volume includes chapters on exobiology in space, chemical and early biochemical evolution, life without oxygen, potential for chemical evolution in the early environment of Mars, planetary protection issues and sample return missions, and the modulation of biological evolution by astrophysical phenomena. Papers are presented on the results of spaceflight missions, the action of some factors of space medium on the abiogenic synthesis of nucleotides, early peptidic enzymes, microbiology and biochemistry of the methanogenic archaeobacteria, and present-day biogeochemical activities of anaerobic bacteria and their relevance to future exobiological investigations. Consideration is also given to the development of the Alba Patera volcano on Mars, biological nitrogen fixation under primordial Martian partial pressures of dinitrogen, the planetary protection issues in advance of human exploration of Mars, and the difficulty with astronomical explanations of periodic mass extinctions.

Schwartz, A. W.↗

NASA NTRS2011

Effect of Microgravity on Sinorhizobium meliloti: Initial Results from the SyNRGE Experiment

SyNRGE (Symbiotic Nodulation in a Reduced Gravity Environment) was a sortie mission on STS-135 in the Biological Research in Canisters (BRIe) hardware to study the effect of microgravity on a plant-microbe symbiosis resulting in biological nitrogen fixation. Medicago truncatula, a model species of the legume family, was innoculated with its bacterial symbiont, Sinorhizobium meliloti, to observe early events associated with infection and nodulation in Petri Dish Fixation Units (PDFUs). Two sets of experiments were conducted in orbit and in 24-hour delayed ground controls. Experiment one was designed to determine if S. meliloti infect M. truncatula and initiate physiological changes associated with nodule formation. Roots of five-day-old M. truncatula cultivar Jemalong A17 (Enodll::gus) were innoculated 24 hr before launch with either S. meliloti strain 1021 or strain ABS7 and integrated into BRIC-PDFU hardware placed in a 4 C Cold Bag for launch on Atlantis. Innoculated plants and uninoculated controls were maintained in the dark at ambient temperature in the middeck of STS-135 for 11 days before fixation in RNA/ate/M by crew activation of the PDFU. Experiment two was designed to determine if microgravity altered the process of bacterial infection and host plant nodule formation. Seeds of two M. truncatula cultivar Jemalong A17 lines, the Enodll::gus used in experiment 1, and SUNN, a super-nodulating mutant of A17, were germinated on orbit for 11 days in the middeck cabin and returned to Earth alive inside of BRIC-PDFU's at 4 C S. meliloti strains 1021 and ABS7 were cultivated separately in broth culture on orbit and also returned to Earth alive. After landing, flight- and ground-grown plants and bacteria were transferred from BRIC-PDFU's into Nunc(TradeMark) 4-well plates for reciprocity crosses. Rates of plant growth and nodule development on Buffered Nodulation Medium (lacking nitrogen) were measured for 14 days. Bacteria cultivated in microgravity in the presence or absence of M. truncatula were characterized by phenotype microarray (PM) analysis of over 1,000 phenotypes including the utilization of carbon, nitrogen, phosphate, and sulfur sources; growth stimulation/inhibition by nutrients, osmolytes, and metabolic inhibitors; and antibiotic susceptibility. (Research supported by NASA ESMD/Advance Capabilities Division grant NNX10AR0

Roberts, Michael S.↗

NASA NTRS1987

A review of recent activities in the NASA CELSS program

A CELSS (Controlled Ecological Life Support System) is a device that utilizes photosynthetic organisms and light energy to regenerate waste materials into oxygen and food for a crew in space. The results of studies with the CELSS program suggest that a bioregenerative life support system is a useful and effective method of regenerating consumable materials for crew sustenance. The data suggests that the operation of a CELSS in space is practical if plants can be made to behave predictably in the space environment. Much of the work centers on the biological components of the CELSS system. Ways of achieving high efficiency and long term stability of all components of the system are examined. Included are explorations of the conversion of nonedible cellulose to edible materials, nitrogen fixation by biological and chemical methods, and methods of waste processing. A description is provided of the extent to which a bioregenerative life support system can meet the constraints of the space environment, and the degree is assessed to which system efficiency and stability can be increased during the next decade.

Macelroy, R. D.↗

NASA NTRS1987

A review of recent activities in the NASA CELSS program

A CELSS (Controlled Ecological Life Support System) is a device that utilizes photosynthetic organisms and light energy to regenerate waste materials into oxygen and food for a crew in space. The results of theoretical and practical studies conducted by investigators within the CELSS program suggest that a bioregenerative life support system can be a useful and effective method of regenerating consumable materials for crew sustenance. Experimental data suggests that the operation of a CELSS in space will be practical if plants can be made to behave predictably in the space environment. Much of the work currently conducted within the CELSS program centers on the biological components of the CELSS system. The work is particularly directed at ways of achieving high efficiency and long term stability of all components of the system. Included are explorations of the conversion of nonedible cellulose to edible materials, nitrogen fixation by biological and chemical methods, and methods of waste processing. It is the intent of the presentation to provide a description of the extent to which a bioregenerative life support system can meet the constraints of the space environment, and to assess the degree to which system efficiency and stability can be increased during the next decade.

Macelroy, R. D.↗

NASA NTRS1999

Mesoscale Eddies, Satellite Altimetry, and New Production in the Sargasso Sea

Satellite altimetry and hydrographic observations are used to characterize the mesoscale eddy field in the Sargasso Sea near Bermuda and to address the role of physical processes on the supply of new nutrients to the euphotic zone. The observed sea level anomaly (SLA) field is dominated by the occurrence of westward propagating features with SLA signatures as large as 25 cm, Eulerian temporal scales of roughly a month, lifetimes of several months, spatial scales of approximately 200 km, and a propagation of approximately 5 cm/s. Hydrographic estimates of dynamic height anomaly (referenced to 4000 dbar) are well correlated with satellite SLA (r(exp 2) = 0.65), and at least 85% of the observed dynamic height variability is associated with the first baroclinic mode of motion. This allows us to apply the satellite observations to remotely sensed estimate isopycnal displacements and the flux of nutrients into the euphotic zone due to eddy pumping. Eddy pumping is the process by which mesoscale eddies induce isopycnal displacements that lift nutrient-replete waters into the euphotic zone, driving new primary production. A kinematic approach to the estimation of the eddy pumping results in a flux of 0.24 +/- 0.1 mol N/sq m (including a scale estimate for the small contribution due to 18 deg water eddies). This flux is more than an order of magnitude larger than the diapycnal diffusive flux as well as scale estimates for the vertical transport due to isopycnal mixing along sloping isopycnal surfaces. Eddy pumping and wintertime convection are the two dominant mechanisms transporting new nutrients into the euphotic zone, and the sum of all physical new nutrient supply fluxes effectively balances previous geochemical estimates of annual new production for this site. However, if biological transports (e.g., nitrogen fixation, etc.) are significant, the new nitrogen supply budget will be in excess of geochemical new production estimates. This suggests that the various physical and biological transport fluxes, as well as geochemical inferences of new production, still need to be reconciled and many outstanding questions remain.

Siegel, David A.↗

NASA NTRS1999

Mesoscale Eddies, Satellite Altimetry, and New Production in the Sargasso Sea

Satellite altimetry and hydrographic observations are used to characterize the mesoscale eddy field in the Sargasso Sea near Bermuda and to address the role of physical processes on the supply of new nutrients to the euphotic zone. The observed sea level anomaly (SLA) field is dominated by the occurrence of westward propagating features with SLA signatures as large as 25 cm, Eulerian temporal scales of roughly a month, lifetimes of several months, spatial scales of approximately 200 km, and a propagation of approximately 5 cm/s . Hydrographic estimates of dynamic height anomaly (referenced to 4000 dbar) are well correlated with satellite SLA (r(sup 2) = 0.65), and at least 85% of the observed dynamic height variability is associated with the first baroclinic mode of motion. This allows us to apply the satellite observations to remotely estimate isopycnal displacements and the flux of nutrients into the euphotic zone due to eddy pumping. Eddy pumping is the process by which mesoscale eddies induce isopycnal displacements that lift nutrient- replete waters into the euphotic zone, driving new primary production. A kinematic approach to the estimation of the eddy pumping results in a flux of 0.24+/-0.1 mol N/sq m/yr (including a scale estimate for the small contribution due to 18 deg water eddies). This flux is more than an order of magnitude larger than the diapycnal diffusive flux as well as scale estimates for the vertical transport due to isopycnal mixing along sloping isopycnal surfaces. Eddy pumping and wintertime convection are the two dominant mechanisms transporting new nutrients into the euphotic zone, and the sum of all physical new nutrient supply fluxes effectively balances previous geochemical estimates of annual new production for this site. However, if biological transports (e.g., nitrogen fixation, etc.) are significant, the new nitrogen supply budget will be in excess of geochemical new production estimates. This suggests that the various physical and biological transport fluxes, as well as geochemical inferences of new production, still need to be reconciled and many outstanding questions remain.

Siegel, David A.↗

NASA NTRS2016

Nitrogen in Ancient Mud: A Biosignature?

Nitrogen is an essential nutrient for all life on Earth and possibly elsewhere. Burial of nitrogen bound to organic matter constitutes the major flux of nitrogen into sediments today, which has led to the inference that nitrogen enrichments in sedimentary rocks may be a biosignature. However, abiotic processes such as lightning or volcanism can fix atmospheric N2 and contribute to sedimentary nitrogen burial in the absence of life. It is therefore uncertain whether observed nitrogen enrichments of up to 430 ppm in Paleoarchean metasedimentary biotite grains are indeed biogenic. This study seeks to address that problem with a numerical model. The NH4(+) concentration of an abiotic ocean is modeled as a function of source fluxes, pH-dependent NH3 volatilization, and equilibrated adsorption of NH4(+) onto clay particles. The results suggest that the observed nitrogen concentrations in Paleoarchean biotite can only be reconciled with purely abiotic processes if the ocean was more acidic (pH <6) and/or if the source fluxes from lightning and volcanism were at least an order of magnitude higher (≥10(exp 12) mol/yr) than previously thought. The bulk of the nitrogen is thus most likely of biological origin. While this does not necessitate a particular metabolism such as biological N2 fixation, the data provide evidence of nitrogen utilization back to 3.8 Gyr. Nitrogen abundances could thus provide useful information in extraterrestrial missions.

Early Earth↗

NASA NTRS2003

Molecular Ecological and Stable Isotopic Studies of Nitrogen Fixation in Modern Microbial Mats

Nitrogen is usually the element limiting biological productivity in the marine environment. Microbial mats, laminated microbial communities analogous to some of the oldest forms of life on Earth, are often the sites of high rates of N fixation (the energetically expensive conversion of atmospheric dinitrogen into a biologically useful form). The N fixing enzyme nitrogenase is generally considered to be of ancient origin, and is widely distributed throughout the Bacterial and Archaeal domains of life, indicating an important role for this process over evolutionary time. The stable isotopic signature of N fixation is purportedly recognizable in organic matter (ancient kerogens as well as present-day microbial mats) as a delta (15)N(sub organic) near zero. We studied two microbial mats exhibiting different rates of N fixation in order to better understand the impact of N fixation on the delta (15)N (sub organic) of the mats, as well as what organisms are important in this process. Mats dominated by the cyanobacterium Microcoleus chthonoplastes grow in permanently submerged hypersaline salterns, and exhibit low rates of N fixation, whereas mats dominated by the cyanobacterium Lyngbya spp grow in an intertidal area, and exhibit rates of N fixation an order of magnitude higher. To examine successional stages in mat growth, both developing and established mats at each location were sampled. PCR and RT-PCR based approaches were used to identify, respectively, the organisms containing nifH (one of the genes that encode nitrogenase) as well as those expressing nifH in these mats. Both mats exhibited a distinct diel cycle of N fixation, with highest rates occurring at night. The delta (15)N(sub organic) of the subtidal Microcoleus mats is near zero whereas the delta (15)N(sub organic) is slightly more positive (+ 2-3%), in the intertidal Lyngbya mats, an interesting difference in view of the fact that overall rates of activity in the intertidal mats are much higher that those in the submerged hypersaline mats. Developing mats in both the subtidal and intertidal locations had delta (15)N(sub organic) values very near those of the established mats. Further work is necessary in order to determine the importance of other transformations of nitrogen on the delta (15)N(sub organic) signature of the mats.

Bebout, B. M.↗

NASA NTRS2017

Nitrogen on Mars: Insights from Curiosity

Recent detection of nitrate on Mars indicates that nitrogen fixation processes occurred in early martian history. Data collected by the Sample Analysis at Mars (SAM) instrument on the Curiosity Rover can be integrated with Mars analog work in order to better understand the fixation and mobility of nitrogen on Mars, and thus its availability to putative biology. In particular, the relationship between nitrate and other soluble salts may help reveal the timing of nitrogen fixation and post-depositional behavior of nitrate on Mars. In addition, in situ measurements of nitrogen abundance and isotopic composition may be used to model atmospheric conditions on early Mars.

Stern, J. C.↗

NASA NTRS2016

Spatial and Temporal Trends in Precambrian Nitrogen Cycling: A Mesoproterozoic Offshore Nitrate Minimum

Fixed nitrogen is an essential nutrient for eukaryotes. As N2 fixation and assimilation of nitrate are catalyzed by metalloenzymes, it has been hypothesized that in Mesoproterozoic oceans nitrate was limited in offshore environments by low trace metal concentrations and high rates of denitrification in anoxic and episodically euxinic deep water masses, restricting eukaryotes to near-shore environments and limiting their evolutionary innovation. To date this hypothesis has only been tested in the Belt Supergroup (∼1.4 Ga), with results that support an onshore-offshore nitrate gradient as a potential control on eukaryote ecology. Here we present bulk nitrogen and organic carbon isotopic data from non-isochronous cross-basinal facies across the Bangemall (∼1.5 Ga) and the Roper (∼1.4–1.5 Ga) basins to better understand the extent and variability of onshore-offshore nitrogen isotope gradients in the Mesoproterozoic. Both basins show an average ∼1-2‰ enrichment in δ-15N(sub bulk) from deep to shallow facies, with a maximum range from ~1‰ offshore to +7.5‰ onshore. Unlike the Belt basin, the Bangemall and Roper basins show some offshore δ-15N(sub bulk) values that are enriched beyond the isotopic range associated with biological N2 fixation alone. This suggests a mixture of aerobic and anaerobic metabolisms offshore. In shallow waters, where δ-15N(sub bulk) enrichment peaks, an aerobic nitrogen cycle was evidently operating. Even though isotopic signatures of aerobic nitrogen cycling are seen in all parts of the Bangemall and Roper basins, our data are consistent with a lateral gradient in nitrate availability within the photic zone, with higher concentrations in near-shore environments than offshore. The variability in δ-15N(sub bulk) values in each depositional environment and the consistently low δ-15N(sub bulk) values from Mesoproterozoic units compared to the Paleoproterozoic and Neoproterozoic suggest that nitrate concentrations in the global ocean were likely low. This trend is now seen in all three Mesoproterozoic basins so far examined, and contrasts with the Paleoproterozoic and Neoproterozoic where nearly all δ-15N(sub bulk) data plot above the N2 fixation window. Thus, we propose that the Mesoproterozoic ocean was characterized by a nitrate minimum, with the lowest concentrations in offshore environments. This inference is consistent with a Mesoproterozoic O2 decline following a temporary Paleoproterozoic O2 peak, and it further supports the idea that nitrate limitation offshore may have contributed to the restriction of photosynthetic eukaryotes to near-shore environments, delaying their rise to ecological dominance until the Neoproterozoic Era.

Mesoproterozoic↗

NASA NTRS2016

Prebiotic Chemistry and Atmospheric Warming of Early Earth by an Active Young Sun

Nitrogen is a critical ingredient of complex biological molecules. Molecular nitrogen, however, which was outgassed Into the Earth's early atmosphere, is relatively chemically inert and nitrogen fixation into more chemically reactive compounds requires high temperatures. Possible mechanisms of nitrogen fixation include lightning, atmospheric shock heating by meteorites, and solar ultraviolet radiation. Here we show that nitrogen fixation in the early terrestrial atmosphere can be explained by frequent and powerful coronal mass ejection events from the young Sun -- so-called superflares. Using magnetohydrodynamic simulations constrained by Kepler Space Telescope observations, we find that successive superflare ejections produce shocks that accelerate energetic particles, which would have compressed the early Earth's magnetosphere. The resulting extended polar cap openings provide pathways for energetic particles to penetrate into the atmosphere and, according to our atmospheric chemistry simulations, initiate reactions converting molecular nitrogen, carbon dioxide and methane to the potent greenhouse gas nitrous oxide as well as hydrogen cyanide, an essential compound for life. Furthermore, the destruction of N2, C02 and CH, suggests that these greenhouse gases cannot explain the stability of liquid water on the early Earth. Instead, we propose that the efficient formation of nitrous oxide could explain a warm early Earth.

Airapetian, V. S.↗

NASA NTRS1996

Evaluation of Cyanothece sp. ATCC 51142 as a candidate for inclusion in a CELSS

Controlled ecological life support systems (CELSS) have been proposed to make long-duration manned space flights more cost-effective. Higher plants will presumably provide food and a breathable atmosphere for the crew. It has been suggested that imbalances between the CO2/O2 gas exchange ratios of the heterotrophic and autotrophic components of the system will inevitably lead to an unstable system, and the loss of O2 from the atmosphere. Ratio imbalances may be corrected by including a second autotroph with an appropriate CO2/O2 gas exchange ratio. Cyanothece sp. ATCC 51142 is a large unicellular N2-fixing cyanobacterium, exhibiting high growth rates under diverse physiological conditions. A rat-feeding study showed the biomass to be edible. Furthermore, it may have a CO2/O2 gas exchange ratio that theoretically can compensate for ratio imbalances. It is suggested that Cyanothece spp. could fulfill several roles in a CELSS: supplementing atmosphere recycling, generating fixed N from the air, providing a balanced protein supplement, and protecting a CELSS in case of catastrophic crop failure.

Non-NASA Center↗

NASA NTRS1979

Studies on the Mechanisms of Microbial Adaptation to the Physical Environment

The environmental factors which affect humans and other animals also influence the microorganisms which are such an important part of our ecology. Some of the microorganisms are very closely associated with animals, living in the digestive tract and synthesizing essential nutrients for the host. For these microbes, most external physical changes are of little consequence, because they are well shielded by the animals' homeostatic systems. The vast majority of microorganisms, however, live free in nature, especially in the soil and oceans. It has been estimated that the upper 15 cm of a fertile soil may contain over 4000 kg of bacteria and fungi per hectare. These organisms are responsible for degrading the complex molecules of plants and animals when they die, eventually producing simple organics, carbon dioxide, and inorganics, which are then used for the next cycle of plant growth. It is believed that over 90 % of the biologically produced carbon dioxide results from the metabolic activity of bacteria and fungi. In addition to recycling plant nutrients, soil bacteria also provide new nutrients through 'fixation' of atmospheric nitrogen into ammonia and nitrate, the forms which can be used by plants. Microorganisms so have an enormous capacity for detoxifying both natural and man-made poisons. All of these functions of microorganisms are essential to the operation of the material cycles on Earth. This is true of all locations on the planet, regardless of the climate or other environmental factors. In fact, one of the most impressive attributes of microorganisms is their ability to adapt to every stable environment on Earth. These include such extremes as polar regions, hot springs, water saturated with salt, mountain tops, ocean depths, acid and alkaline waters, deserts, intense radioactivity, soil and water contaminated with toxic chemicals or petroleum, and areas devoid of oxygen.

Heinrich, M. R.↗