Our hypothesis is that the great majority of Magnéli phases in the environment are derived from TiO 2 minerals present in coal. This is strongly suggested by both the circumstantial evidence presented above concerning the spatial and temporal relationships between Magnéli phases and coal-fired power plants (over 1000 °C, locally reduced environments resulting from areas of incomplete combustion in the firebox), as well as the synthesis of Magnéli phases under the conditions of our heating experiments (over 900 °C, TiO 2 with pulverized coal under a N 2 atmosphere). It is also important to consider the possibility of generating Magnéli phases during coke production. Coke, typically made under highly reducing conditions from low-sulfur, low-ash bituminous coal at temperatures similar to those used in this study (over 900 °C), should result in Magnéli phases production. As mentioned in the Introduction, coke made from coal is used to produce 70% of the world’s steel.

TiO 2 naturally occurs in coal as anatase, rutile, and brookite, the three mineral TiO 2 polymorphs, whereas Magnéli phases have never been reported in any rank of coal, or coal origin. In summary, Swaine30 summarized Ti associations in coals, noting that Eskanazi31 called for an organic association of Ti. While an organic association may be the case in peats and low-rank coals, Finkelman11 found anatase and rutile in bituminous coals. Ketris and Yudovich12 acknowledge this mixed affiliation, placing Ti among the weakly or moderate coalphile elements. The levels of TiO 2 in coal vary, but generally are found within a range from roughly a few tenths of a percent, to a few percent, by weight. For example, Hower and Bland13 and Hower et al.14. found the TiO 2 content in the Pond Creek coal in eastern Kentucky to vary between 0.13–6.52%, with the highest amounts found in association with relatively high concentrations of Zr (as zircon, ZrSiO 4 ) in clastic-origin lithotypes. Similar trends were noted in eastern Kentucky’s River Gem15 and Elswick16 coals.

It should be noted that we have considered the possibility that Magnéli phases result from TiO 2 polymorphs, especially anatase, due to its common use in the catalytic beds of modern coal-fired power plants in the combustion gas exhaust stream. These beds are designed to minimize/eliminate NO x in the exhaust stream, commonly using anatase/rutile to provide favorable chemical conversion of these toxic emission gases present depending on the type of coal that is burned. Any release of the titanium oxides in the gas stream during years of service would be trapped by the plant’s electrostatic precipitators along with the fly ash exhaust component that it is designed to collect. However, such a scenario does not account for two factors. First, anatase/rutile used in these catalytic beds (e.g., P25) lack Magnéli phases. Second, the temperature of gases in this part of the power plant are many hundreds of degrees too low to generate Magnéli phases. Temperatures of at least 900 °C were needed in this study to convert anatase/rutile to Magnéli phases, with that temperature easily exceeded in the combustion chamber of a power plant. Therefore, TiO 2 used in catalytic beds should not be a source for titania suboxides from coal-burning power plants.

It should also be noted that burning municipal solid waste is becoming more and more common worldwide, and the production and/or fate of nanoparticles (including TiO 2 in commercial products) during this incineration is of growing interest (e.g., refs 32, 33). Many incineration protocols use temperatures below what we have found to be conducive to Magnéli phase production under highly reducing conditions (<900 °C). In addition, our preliminary experiments to date using P25 starting material in the presence of sewage sludge under N 2 at 900 and 1000 °C produced rutile exclusively (as measured by powder XRD). However, some incineration is driven by burning coal at temperatures well in excess of 1000 °C, and here we would expect the production of Magnéli phases both from the TiO 2 in the coal itself and any in the waste. Given a 2014 estimate that 8600 metric tons of nanomaterials are incinerated annually on a global basis34, and that TiO 2 nanomaterials would be some fraction of this, and that high temperature incineration using a carbon-based fuel would be some fraction of this, the production of Magnéli phases due to incineration is several orders of magnitude less than our estimated Gt levels of Magnéli phase generation due to industrial coal-burning (see Discussion below). Therefore, waste incineration is not expected to be a significant contributor to Magnéli phase production relative to coal-burning power plants.

Schindler and Hochella35 very recently identified Magnéli phases in soils proximal to Cu-Ni-sulfides smelters and refineries in Sudbury, Ontario, Canada. Although the identified nano-size Magnéli phases only occurred as minute traces of material in mineral surface coatings, its discovery in this setting suggests that these phases can also form during the reductive smelting and refining of metal-bearing ores in the presence of coke, coal, or carbon monoxide. In this scenario, this also opens the possibility of Magnéli phases originating from TiO 2 polymorphs present in the ore being smelted and refined. Hence, the anthropogenic formation of Magnéli phases may not be limited to coal-burning power plants and likely also coking facilities. Nevertheless, further study is needed, and this paper has concentrated on coal-burning power plants due to their tremendous and still growing abundance in the industrial world.

With the seeming ubiquity of incidental Magnéli phases from coal combustion, in fact it is quite the opposite for naturally occurring Magnéli phases. Such naturally occurring instances are very rarely recognized. Magnéli phases have infrequently been observed in lunar rocks, as oxygen deficient, blue “rutile”36, 37. Further, Magnéli phases have been suspected or identified, for example, as rare Ti oxide phases in interplanetary dust particles38, in carbonaceous chondrite meteorite matrices39, and in micrometeorites in Antarctic ice particles40. Aside from these extraterrestrial origins, the only Earth-bound natural occurrence that we could locate in the literature comes from Pedersen and Rønsbo41 who discovered “mudstone xenoliths” exposed in one location on the central coast of western Greenland where andesitic magma likely flowed into shallow water underlain by a carbonaceous mudstone, resulting in high temperature (about 1200 °C), low confining pressure (close to five bars), extremely reducing (producing native iron), pyrometamorphosed sediment xenoliths where anatase/rutile grains were transformed to Magnéli phases.

Given our assessment that the overwhelming majority of nanoscale Magnéli phases found in the environment are from industrial coal-burning, it is possible that these Magnéli phases could be used as a tracer for the global distribution of coal-burning solid-state emissions. Scientists have been working on using various source apportionment techniques for tracking coal-burning emissions using isotope geochemistry, chemical fingerprinting, and modeling to differentiate coal ash contamination from other contaminant sources in the environment (e.g., see refs 42,43,44). This is a very difficult task due to the extraordinary complexity of environmental chemistries and physical matrices. A unique fingerprint to trace the distribution of coal ash components around the globe is still lacking. More specific tracers are also needed for medical diagnoses, especially in the study of lung disease due to the severity of this problem as discussed in the Introduction of this article.

Therefore, Magnéli phases are presented here as a new tracer candidate for coal-burning power plant and likely coke production/smelting plant emissions, both fluvial and aeolian. Such a tracer could be used alone, or in combination with other source apportionment techniques mentioned above. Perhaps the strength of a Magnéli phase tracing method is in its surprising simplicity and ease of use. This stems from the confluence of a number of fortunate occurrences and processes that work together to provide such a method. TiO 2 mineral phases are essentially a ubiquitous accessory phase in all coals worldwide, generally varying from a tenth of a percent to several percent, by weight. Combustion of the coal, with included TiO 2 minerals which are never intentionally targeted for separation from the coal due to their relatively benign nature, and at temperatures over 1000 °C under locally reducing conditions, very quickly produces Magnéli phases. Although worthy of a separate study, the grain sizes of the Magnéli phases generated should be quite variable, although in this study, using TEM as the critical identification and tracking tool, we have selected for submicron grains. These Magnéli phases are then entrained with the many other gaseous and condensed matter components of the plant emission stream. Some fraction of these phases will leave the plant with the gaseous stream (from virtually none to a significant proportion, depending on the plant design and efficacy of its emission-control systems). The remainder will end up in the collected ash components, to be later stored in impoundments or landfills, or recycled into various ash-containing products (concrete/cement, wallboard, road fill, etc.). In all of these possibilities, the incidentally produced Magnéli phases are entering some aspect of the environment, and are immediately or eventually (through secondary processes, e.g., wallboard disposal in a landfill, or incinerated) subject to transport via natural aeolian or fluvial process, and often a combination of the two.

The organismal and ecological environments that these Magnéli phases enter lack the occurrence of Magnéli phases, given their extraordinary rarity in natural systems. On the other hand, we estimate the production of Magnéli phases due to industrial coal-burning to be enormous over the last two centuries since the Industrial Revolution. Considering ballpark, but well-founded estimations of coal productions in modern times1, accounting for the great majority of coal that has ever been used, one can say that on the order of a few hundred gigatons (Gt) of coal has been burned by humans. We can also estimate from existing observations and data that coal contains on the order of an average of 2% TiO 2 , and that, on average, a coal will produce roughly 15% residual ash (both of these estimates are ours, from our personal estimations from the vast coal mineral and ash literature, and our own experience). While the conversion efficiency of TiO 2 minerals to Magnéli phases in the burning process is not known, we can say that, at least in the size range of up to several hundred nanometers (as observed in this study among 22 ashes collected from around the United States and China), most of the titania has been converted to Magnéli phases.

Considering all of this, we are still left with on the order of a Gt of Magnéli phase production via industrial coal-burning over the last few centuries to be spread via the atmosphere and hydrosphere around the planet. The bottom line is that if one observes these highly unusual, easily recognizable phases in selective searching with a TEM, whether in or on soils, river/estuary water or sediments, city streets, stormwater ponds, human lung tissue, or wherever else, that portion of the environment has been very likely impacted by these phases and other solid state components in a similar size range from the sources that have been described herein. The reach of these small physical components (e.g., naturally occurring nano-sized inorganic solids) is global, as is well-known and documented10.

Until now, and as described in detail above, titania suboxides were not known to be widely distributed in the environment, and to our knowledge have not been used in commercial products with wide distribution20. This explains why toxicity testing had not been initiated and underscores why an understanding of the particles’ toxicity potential is now needed. In comparison, the nanoparticles of the polymorphs of TiO 2 are widely used in commercial products, from paints to makeup to sunscreens, among other uses, and as expected, the toxicity of these nanoparticles have been widely studied. TiO 2 nanoparticle toxicity has been extensively examined in the context of freshwater and marine environments and in organisms belonging to several trophic levels45,46,47,48. It is generally thought that oxidative stress is the primary mechanism of acute toxicity to developing organisms due to the ability of forms of TiO 2 to produce reactive oxygen species (ROS) when irradiated49,50,51,52. ROS leads to cell death via protein, lipid, and DNA damage45, 46, 48. There is also evidence that sub-chronic exposure to adult zebrafish causes neurological effects associated with spatial recognition memory and behavior52. Several studies implicate TiO 2 nanoparticle coating, shape, size, and aggregation properties as confounding variables to these nanoparticle’s bioavailability and toxicity45, 46, 50, 53. This is especially relevant in studies using zebrafish models because of the protective chorion (an acellular enclosure) encompassing the developing fish between 0–48 hpf. Though its permeability has not been thoroughly characterized, the zebrafish chorion is a known barrier to the uptake of many contaminants, including metallic nanomaterials29, 54,55,56,57. Studies aiming to characterize the toxicity of metal nanoparticles commonly remove the chorion prior to exposure to ensure particle bioavailability during early stages of development when organisms are most sensitive to environmental stressors29, 54, 56, 57. In fact, in additional experiments with chorionated zebrafish embryos in this study (data not shown), we failed to observe significantly reduced survival after exposure to P25 and P25-900 °C nanoparticles at concentrations up to 1000 ppm; these results corroborate the references cited above, demonstrating the protective effect of the zebrafish chorion barrier to titanium oxide nanomaterial bioavailability. The chorion is also commonly removed in screening assays investigating the toxicity potential of pharmacological agents or other chemicals; for these purposes, the dechorionated embryonic zebrafish is a high-throughput and robust vertebrate model54, 56, 57.

Therefore, in this first study of titania suboxide toxicity, we were primarily interested in reporting the inherent toxicity of the P25-900 °C (Magnéli phase) particles in the absence of the embryonic zebrafish protective chorion barrier (i.e., toxicity relevance to aquatic animal gills or terrestrial animal lungs). We observed significant reductions in embryo survival following acute exposure to these particles in the absence of SSR, but not following co-exposure to P25-900 °C and SSR. These results are in stark contrast to those of P25, in which the detrimental effects are primarily attributed to the material’s photo-induced toxicity due to the generation of ROS as described above. In contrast, the reason for the toxicity of Magnéli phase titania suboxides is not known, this being the first time that a formal biotoxicity study has been conducted for these materials. Whatever role Magnéli phases play in and around biological systems is expected to be fundamentally different than TiO 2 phases. Unlike the wide band gap semiconducting, UV absorbing TiO 2 phases, Magnéli phases are narrow band gap semiconductors (see above), with electrical conducting properties similar to carbon/graphitic materials20. Additionally, these variably defective materials are expected to have interesting and important ionic conductivity and catalytic properties that still need to be thoroughly explored.

The immediate relevance of this work is aquatic organism exposure under conditions of limited solar radiation co-exposure, but there are also translational implications for human health. Of particular interest is the reactivity of Magnéli phases in human lung alveolar membranes considering their accessibility to this critical and vulnerable portion of our physiology, and the fact that their biological reactivity likely does not depend on solar radiation co-exposure.

Overall, Magnéli phases are a newly recognized incidental nanomaterial in the environment with very wide distribution, allowing it to be a new candidate for tracing the distribution of industrial coal-burning solid-state emissions worldwide. In addition, while we provide an initial assessment of Magnéli phase toxicity using an established exposure regimen and animal model, this situation also clearly invites further toxicity studies aimed at comprehensive characterization of Magnéli phase toxicity at sublethal concentrations and investigations of potential mechanisms of action. New toxicity pathways in micro- to macro-organisms, including humans, are likely to be found.