THRIVING ON LIFE-MINERAL COEVOLUTION Behrooz Abbasi, Vahid Nasiri, Babak Azarfar, Kyle Riemenschnitter

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Behrooz Abbasi, Vahid Nasiri, Babak Azarfar, Kyle Riemenschnitter. BIOMINING THRIVING ON LIFE-MINERAL COEVOLUTION. 2021. ￿hal-03181771￿

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Behrooz Abbasi*1, Vahid Nasiri1, Babak Azarfar1, Kyle Riemenschnitter1

1Department of and Metallurgical Engineering, University of Nevada, Reno, 89557, USA

*Corresponding author’s email: [email protected]

ABSTRACT

The history of biomining is very broad and rich, starting from the evolution of stars and planets to the coevolution of terrestrial life and minerals. In this paper, we briefly review the origin of elemental and compositional diversity of minerals and how microorganisms and plants connect mineralogy to biology. Thereafter, we revisit biomining from the perspective of its fundamental elements, limitations, and unexplored potentials. Finally, we make a number of indicative remarks with respect to those limitations and potentials to emphasize an existing need for the emergence of a sustainable biomining and prevent its premature application.

KEYWORDS

Life-mineral coevolution; microorganisms; bioextraction, low-grade minerals

BIOMINING: LIFE-MINERAL COEVOLUTION

As the manifestation of biology-mineralogy nexus, biomining is concerned with coevolution

(and coexistence) of terrestrial life and minerals, which entails the evolution of the Earth’s geosphere, biosphere, and atmosphere, and is in turn entailed by the formation of the Earth (and stars) [1]. Minerals are the most trustworthy testifiers of the history of the Earth; a terrestrial mineral could narrate a history of up to 4.5 billion years (and more) about the Earth (and the

Universe). In a sense, (roughly) unaffected minerals freeze a period of history that is relatively unique to mineralogy, even compared to astrophysics which is based on retrospective observations. The upper 3 kilometers of Earth’s surface is where biology and mineralogy actively interact [2]. Besides epistemic benefits behind the history of life-mineral coevolution, biomining can take practical advantages of analyzing that history [3]. Although there is no firm consensus on the very definition of the term “(co)evolution” in the scientific literature, in this paper, it refers to spaciotemporal changes which promotes complexity and diversity. Moreover, the earlier steps of evolution are logically followed by the latter steps; there is a sequence of events rather than randomness. This logical sequence can be understood in a retrospective manner and not necessarily in a predictive manner. This definition of evolution is applicable in the context of minerals which may not be in full agreement with biological definition of evolution [4]. Yet, it is extendable to biology by including competition, mutation, and inheritance.

Strong evidences support this hypothesis that the oldest terrestrial minerals/life were formed earlier/later than the formation of the Earth [5,6]. While this could suggest minerals to be primitive and life to be derivative, the two are intimately connected; life depended on minerals to first form and minerals depended on life to coevolve. Nonetheless, the elemental diversity of both terrestrial minerals and life mainly stems from stellar nucleosynthesis within stellar evolution [7]. As a rule of thumb, the larger the star is, the heavier the elements that could be formed within stellar nucleosynthesis [7]. However, formation of elements after , with the highest nuclear stability, is not energetically favorable even for large stars, and typically are made via explosion of large stars known as supernova (Figure 1) [8]. Eventually, these elements either participated in the formation of the Earth (majority) or were later on transferred by means of mediators such as comets (minority). Thereafter, chemical processes, revolving around

(transferring/sharing) electrons, followed by biochemical processes mainly took over to create diversity of minerals and their chemical composition. H He 1,-1 Li Be B C N O F Ne 1 2 3 4,-4,2 3,-3,5 -2 -1 Na Mg Al Si P S Cl Ar 1 2 3 4 6,-2,2 1,-1,3 K Ca Sc Ti V Cr Mn Fe Co Ni Cu Zn Ga Ge As Se Br Kr 1 2 4,3 5,4,3 3,2,6 2,3,4 2,3 2,3 2,3 2,1 2 3 3 4,-2,6 1,-1,5 Rb Sr Y Zr Nb Mo Tc Ru Rh Pd Ag Cd In Sn Sb Te I Xe 1 2 4 5,3 6,5,4 7 3,4,6 3,2,4 2,4 1 2 3 4,2 4,-2,6 1,-1,5 Cs Ba Hf Ta W Re Os Ir Pt Au Hg Ti Pb Bi Po At Rn 1 2 4 5 6,5,4 7,-1,6 4,2,3 4,2,3 4,2 3,1 2,1 1,3 2,4 3,5 4,2 1,-1,3 Fr Ra 1 2 La Ce Pr Nd Pm Sm Eu Gd Tb Dy Ho Er Tm Yb Lu 3 3,4 3,4 3 3 3,2 3,2 3 3,4 3 3 3 3,2 3,2 3 Ac Th Pa U Np Pu Am Cm Bk Cf Es Fm Md No Lr 3 4 5,4 6,5,4 5,4,3 4,3,5 3,4,5 3 3,4 3

Figure 1. Origin of elemental diversity of minerals; cosmic rays/Big Bang (white), stars/supernova (yellow), manmade (red; these are very short-lived, created only in labs). The numbers below each element correspond

to its oxidation state(s).

Coevolution of minerals and life is a consequence of numerous positive and negative feedbacks.

A mineral is a crystalline compound that has a regular atomic structure, and has a well-defined chemical composition [9]. As far as mineralogy is concerned, this coevolution affects mineral diversity/distribution, which in turn is affected by how various factors (e.g., physical, chemical, and biological) have changed that diversity/distribution [4]. Mineralogy includes variations in chemical compositions, sizes, and shapes (morphology) with a main focus on near-surface environment [9]. The concentration of mineral forming chemicals has to be high enough for them to bind together and create minerals, and the ambient temperature should be low enough for the mineral to be condensed [4]. As the supernova envelope expands, cooling of carbon rich regions provides the minimum concentration and maximum temperature in which crystallization of any known mineral could possibly occur. Hence, diamond nanocrystals are speculated to be the first minerals that could be formed in 4000 K in the carbon rich zones of supernova envelopes via what is called vapor deposition. About 400 K below 4000 K, the condition is suitable for the formation of another allotrope of carbon; i.e., graphite [4]. Diamond and graphite (C), and 10 other pre-solar nanocrystals are the earliest minerals formed in the cosmos, and still ubiquitous everywhere; constituting a total number of 12 minerals known as Ur minerals, namely moissanite (SiC), osbornite (TiN), nierite (Si3N4), rutile (TiO2), corundum (Al2O3), spinel

(MgAl2O4) hibbonite (CaAl12O19), forsterite (Mg2SiO4), GEMS (silicate glass with embedded and ), and metallic nanoparticles (e.g., TiC, FeC, and Fe-Ni) within graphite [10].

The Ur minerals are formed from 1) the most abundant elements formed in stars and 2) elements which can form crystals at very high temperatures. 10 elements satisfy those requirements, namely carbon, silicon, nitrogen, titanium, , calcium, aluminum, iron, , and oxygen. We shall see how those 12 Ur minerals with only 10 different essential elements have evolved to >5000 minerals (5603 is the most recent value based on the IMA database of mineral properties) with >70 different essential elements on Earth with the aid of biology [11].

Diversity of minerals increase from 12 to 60 minerals within the formation of the solar system by fusing the Ur minerals within melting cycles to form the early chondrite minerals. Those chondrite minerals start clumping together to form planets with metallic cores and silicate mantles, resulting in further diversification of minerals up to ~250 under abrupt changes, such as thermal bursts and shock waves [2,12]. Also, the elemental diversity in minerals increases from

10 to 20 within the latter stage; all along this evolution, complexification occurs as previously stated. It should be emphasized that primitive chondrite meteorites included the elemental diversity (>70) required for the mineral diversity of the modern Earth (>5000), but most of those elements were too rare/disperse [4]. Mineral diversity of dry planets, such as mercury, has ceased about 250-300. On wet planets, such as Mars, this value is speculated to be as high as 400, owing to hydrological impacts. However, Earth has enough internal heat to undergo more melting cycles to concentrate some rare elements, such as , cesium, and niobium, within granite formation [4,13]. Purification through a number of those melting cycles forms a very specific type of minerals called pegmatites; increasing the mineral diversity up to ~1000. Dating the oldest pegmatite (about 2.8 billion years), it can be deduced that the later stage took more than a billion years to perform those physicochemical purifications [4,14]. Being unique to Earth, plate tectonics is a major physicochemical contributor to mineral diversity (increasing it up to 1500), where the upper layer is denser than its lower layer and is drawn down by gravity, reprocessing a huge volume of the Earth crust [13]. This includes crystallization of the high-pressure minerals, such as diamond. It has been hypothesized that all the aforementioned minerals could have played significant roles in the formation of life [2,4]. This is from protecting prebiotic molecules and catalyzing the prebiotic processes to serving as scaffolds (to assemble smaller molecules into macromolecules) and providing selective surfaces (to concentrate chiral molecules and seed chiral life) [15,16]. We further discuss that life (and biological processes in general) in turn is the missing piece which fills the significant gap between ~1500 (formed by physicochemical processes) and >5000 minerals existing on the modern Earth.

Life per se neither adds any new minerals to the existing list prior to its formation nor introduces any new chemical process, but rather it catalyzes the reactions which would have been kinetically unfavorable in its absence [2,5]. For instance, microorganisms get their energy from chemical transformation of minerals in exchange for expediting those transformations, and that is the basis of coevolution of life and minerals. In such process, microorganisms use enzymes, in which active sites have evolved for oxidation reduction (electron transfer) reactions required for metabolic processes [5]. Those active sites reflect the chemical environment that microorganisms are evolved in, e.g., formation of iron-rich active sites indicate the chemical composition of the oceans on the early Earth. About 2.5 billion years ago, cyanobacteria started changing the chemistry of the Earth’s atmosphere by using the Sun’s energy and producing oxygen, i.e., oxygenation stage [5,17]. The latter contribution from biology to mineral diversity on Earth is more than any other previously mentioned contribution from solo physicochemical processes [5].

Supported by experimental evidence, it has been hypothesized that mineral diversity has drastically increased as the result of oxygenation of the Earth’s atmosphere [5,17]. This is evidently mirrored in the chemical composition of the minerals before and after the oxygenation stage. For instance, most of the iron, nickel, manganese, , and uranium minerals (and many more) owe their existence to life [2,5,17]. After the oxygenation stage, iron was diluted away and molybdenum became more abundant in the oceans. This evolution of oceanic geochemistry is reflected by evolution of biological enzymes as well [18,19]. For example, nitrogenase enzymes (responsible for nitrogen fixation) have adopted iron-rich/ molybdenum- rich active sites before/after the oxygenation stage [20]. Moreover, after the oxygenation stage, higher oxidation states of elements such as rhenium became soluble, and thus could penetrate to subsurface regions and participate in molybdenum minerals [21]. This can be deduced from increasing the trace of rhenium in molybdenum minerals along with increasing the concentration of atmospheric oxygen in time [21]. The other significant variation in the atmospheric composition occurred in the ice age where greenhouse gases (e.g., CO2) were gradually accumulated and mineral diversification ceased. Formation of the terrestrial biosphere coincided with the formation of biominerals, such as abelsonite and evenkite, as well as an increase in the formation of clay minerals [22]. Living components, such as plant’s roots, microorganisms, and worms mainly participated in the breakdown of rocks and extraction of their nutrients. In all the aforementioned stages, life has also affected the morphology of minerals [23]. For example, old uranium deposits (pre-life) are larger crystals of uranium oxide, while modern deposits (post- life) are mainly formed as nanocrystals [13,24]. Taken together, life has left its footprints from chemical composition (as in copper oxides) to morphology of minerals (as in uranium deposits) on Earth.

From the periodic table, 8 elements have more than 98% contribution in the structure of minerals on Earth, namely oxygen, silicon, aluminum, iron, calcium, sodium, potassium, and magnesium

[25]. Life on the other hand is mainly based on hydrogen, carbon, oxygen, and nitrogen, and thus has to fulfil most of its needs from the Earth's atmosphere [26]. Hydrogen and oxygen can be exchanged between the Earth and its atmosphere mainly through the physical processes of the hydrological cycle; evaporation, condensation, precipitation, infiltration, surface runoff, and subsurface flow [27,28]. While nitrogen/carbon is exchanged within biochemical processes in plants and microorganisms via nitrogen/carbon fixation [29,30]. Competition between living species requires taking advantage of the fast kinetics of electron-transfer processes, which in turn is enhanced by metal ions existed in minerals [31]. Bioextraction of these is what biomining is all about as will be discussed in the following.

BIOMINING: SCIENCE AND TECHNOLOGY

Biomining is one of the broadest multidisciplinary topics where science (e.g., biology, geology, chemistry, and physics) and engineering (e.g., mining, metallurgical, and mechanical) meet. On one hand, biomining priorly deals with fundamental factors (e.g., physicochemical, microbial, and mineral factors; Figure 2). On the other hand, it posteriorly has direct and mutual impacts on the market and the environment. Although biomining is defined as extraction of minerals

(metals) by the virtue of microorganisms [32], both bio and mining have much broader domains.

For instance, there is no fundamental distinction between biomining and algal-bacterial wastewater treatment in the sense that both increase the concentration of their target of interest with the aid of living beings [33]. As a branch of science, biomining is a subdivision of , which has been partially used in the mining industry. However, majority of biohydrometallurgy subdivisions, such as biobeneficiation, biofloatation, and biocoagulation are yet to be commercialized [32]. Biomining itself has two subdivisions, namely biooxidation and that are profitable for low-grade minerals (e.g., aurostibite) and secondary resources

(e.g., landfill and waste dump) at their current stage [34]. Although biooxidation literally refers to oxidation of metals with microorganisms (that is predominant in bioextraction), it is historically named after dissolution of the matrix around the target metals, while bioleaching is used for dissolution of the target metals, making the latter more selective [34,35]. While passive bioleaching is a term used for bioextraction processes occurring once the mine waste is deposited at the surface. Selective approaches are more desirable for extraction of metals from exponentially growing low-grade resources, where the terms “biomining” and “bioleaching” are often interchangeably used [35]. Nonetheless, biomining has also been successfully employed at the largest copper mine of the world, i.e., Escondida in Chile where high-grade resources exist

[35,36].

Biotransformation • Strain • Microbial diversity Biocoagulation • Microbial interactions • Population density • Activity Prospective Biocoagulation Microbiological • Spatial distribution of y microorganisms g factors r • Metal tolerance

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l n Waste dump Landfill • Adaptation ability

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m c Bioflotation Bioleaching

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p Biomining Mineral

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A h Mine Biooxidation factors Physicochemical

o i Commercial

B • Mineral type factors Waste water • Composition Sulfate Reducing Prokaryotes (SRP) • Temperature treatment • Particle size • pH • Surface area • potential In-use • Porosity • O2, and CO2 • Leaching mode • Resource Biobeneficiation • Solids availability- concentration nutrients • Stirring rate • Fe2+, and Fe3+ • Tanks in series Laboratory-scale Biosensoring • Inhibitors • Particle shearing • Heavy metals • Presence of other metal • Turbidity Coal • Salinity desulfurisation • Light

Figure 2. Biomining as a subdivision of biohydrometallurgy and its essential components Typical extractive techniques include several expensive steps such as smelting, roasting, and pressure oxidation, which are environmentally unfriendly and demand high concentrations of elements as the input [59,60]. However, microorganisms often gain energy by breaking the bonds between constituent elements of minerals. As the result, energy intensive components of traditional mining (e.g., grinding and extraction) become energetically favorable. Moreover, bioextractive methods do not involve digging, transporting, and disposing of large amounts of rock, unlike in traditional mining. Finally, mineral-feed weakening and breakage (i.e., crushing, grinding and pulverizing) is commonly the most energy consuming and expensive step in traditional mining process taking up to 80% of the total energy consumption [62]. This becomes more highlighted considering the fact that mining sites are usually not connected to the grid; feeding on energy intensive environmentally unfriendly diesel generators [35]. However, bio- assisted pretreatment can enhance the grinding efficiency of mineral . The basis of this approach is that microorganisms are capable to affect rock structure through their activities during weathering process. Microorganisms, such as fungi, are significant geoactive agents that are able to modify the surface structure and chemistry of rocks [63]. These microorganisms can survive with extreme moisture and temperature fluctuations on rock surfaces where limited nutrient is available. It has been reported that certain microorganisms, such as lichen, can accelerate the rock weathering process by an order of magnitude [64,65]. Different from the naturally occurring process, the weathering involved with microorganisms seem to leave the rocks with different microstructures. Such example is evident where grooves along the mineral grains were created due to the activities by fungal hyphae [66].

In a broader academic/industrial range, microorganisms have been used in bioextraction of all sorts of elements for three main purposes: 1) increasing the concentration of target metals in the solution, i.e., dissolution, 2) decreasing the concentration of target metals in the solution, i.e.,

precipitation, and 3) removing environmentally unfriendly components, i.e., decontamination.

Those microorganisms include bacteria (operational pH = 0-3), (operational pH = 0-5),

and fungi (operational pH = 3-9), which are typically extremophiles (e.g., acidophiles and

). In terms of metabolism, typical microorganisms used in biomining are

chemolithotrophs (bacteria), heterotrophs (fungi), or facultative anaerobes (bacteria and archaea)

[35,37]. Table 1 represents a number of microorganisms with the capability of bioextraction of

metals at small academic scales (mainly transition metals). This bioextraction occurs via cell

metal intake, secretion of organic acids, or metabolic use of metal in (an)aerobic respiration

[38,39]. Traditional microbiological techniques are based on isolating and studying

microorganisms existing in in-situ samples. However, only about 1% of those microorganisms

can be isolated in the lab. On the other hand, genomic techniques rely on extracting the DNA of

domestic microorganisms and copying their genome to develop those species that are naturally

adapted to specific environmental conditions. While the ecological impacts of the modified

genes are yet to be determined, none of the industrially-used microorganisms are known to be

pathogenic.

Table 1. Different microorganisms (bacteria and fungi) for bioextraction of metals [31,32,35,40–55]

Archaea Metal Bacteria Metal Fungi Metal

Iron At. ferrooxidans Copper Copper Aspergillus niger Tin At. Thiooxidans

Leptospirillum ferriphilum Acidianus copahuensis Zinc Aspergillus niger Cobalt ferrooxidans

Thiobacillus Acidianus copahuensis Copper Gold Penicillium simplicissimum Nickel spp

Acidithiobacillus Nickel Cladosporium Acidianus copahuensis Copper Leptospirillum Gold Copper cladosporioides Sulfobacillus

Acidianus copahuensis Zinc At. Thioooxidans Nickel Penicillium simplicissimum Aluminum

L. ferriphilum Acidianus copahuensis Cadmium Copper Aspergillus niger Mercury A. caldus

Crenarchaeota Gold Acidithiobacillus ferrooxidans Uranium Aspergillus niger Lead

Acidithiobacillus caldus Copper Euryarchaeota Gold Penicillium simplicissimum Zinc Sulfobacillus thermosulfidooxidans Silver

In contrast to the conventional hydrometallurgical techniques, recovery of metals by biological

processes is considered a “clean technology,” which is based on the interactions between

microorganisms and metals under mild operating conditions, leaving strikingly less carbon

footprints behind [35]. Biomining is mainly allocated to extraction of copper and gold at the

industrial scale [35]. In the case of metals such as gold, which are expensive and naturally exist

in low concentrations, the lower cost of bioleaching outweighs the required time in extractive

. Low concentration of target metals is not challenging for microorganisms as they

simply ignore what is not considered their food, resulting in high extraction yields; more than

90% in some cases. On top of dealing with low-grade ores, traditional gold mining includes

− cyanidation which produces aurocyanide complexes, Au (CN)2 ; in turn binding to carbonaceous

compounds present in the gangue material and becoming unrecoverable [58]. Microorganisms

can be used to prevent the bond between aurocyanide and carbonaceous compounds initially, or

can be used to break that bond in the and release the gold [58]. However, biomining needs to be extended to other minerals, such as rare earth elements (REEs), where the low-grade and high industrial demand has rendered traditional mining difficult and expensive. The word

“Rare” refers to dispersity (as opposed to low abundance) of REEs, making them profitable targets for biomining. Especially, the recent discovery on the role of Ce3+ and La3+ in oxidizing methanol to carbon and energy has drawn interests in biomining of REEs [56,57]. Traditional methods could be replaced by bio-assisted concentration at different stages of biomining of

REEs as follows.

In the main stage of biomining (excluding mineral pre-/post-processing), microorganisms are used for liberation and/or separation of target metals. Separation processes can be biological,

(electro)chemical, and/or mechanical. Biosorption, bioaccumulation and bioprecipitation are three microbial strategies to separate target metals (Figure 3, stage 3). If there are multiple target metals in a sample (natural or artificial) a proper combination of physicochemical and biological strategies should be employed. Figure 3 shows a schematic representation of bioleaching, sulfidogenic, electrochemical selective extraction, and chemical extraction (bio)reactors, in which physicochemical and biological processes recover 8 metals in 4 stages. In stage 1, the use of zero-valent sulfur (ZVS) can be used to increase bioleaching efficiency as many acidophilic bacteria and archaea commonly use ZVS as an electron donor [67]. In an aerobic environment, oxidation of ZVS combined with reduction of molecular can decrease the pH by generating sulfuric acid. On the other hand, in an anaerobic environment, the oxidation of ZVS can be combined with the reduction of ferric iron with the aid of some acidophiles [67]. These acidophiles are often autotrophs, which in turn reduce the carbon footprints of bioleaching. For instance, the autotrophic Acidithiobacillus species have been commonly-used for bioleaching of metals. However, most secondary sources have alkaline nature and/or toxic heavy metals, making the growth of acidophiles extremely difficult. Although some indigenous acidophiles have been successfully used for bioleaching of copper and iron from secondary resources more researches required to adapt microbes to alkaline environments. Sulfidogenic bioreactors (Figure

3, stage 2) can be used as a source of hydrogen sulfide to selectively precipitate copper and zinc, in the form of copper/zinc sulfide in a lower/higher pH. Selective precipitation becomes highly beneficial in metal recovery from mine drainage resources which have low concentrations of aqueous metals. While electrochemical processes are considered to be very selective in separation of some transition metals (e.g., copper, zinc, and nickel), they cannot practically reduce REEs. Therefore, a proper combination of precipitation and electrochemical methods could be employed based on the chemical composition of the solution. The metal containing leachate can be introduced to an electrochemical cell (Figure 3, stage 3) or undergo further biological processes (e.g., biosorption, bioprecipitation). Bacillus subtilis and Escherichia coli have been used in such biological processes for extraction of light and heavy REEs (La, Ce, Y,

Pr, Nd, Tm, Yb and Lu) [68]. REEs can be precipitated via the phosphate group released by microorganisms. Elements such as silver and gold can be recovered using (bio)chemical leaching. Cyanogenic bacteria have been commercially used for bioleaching of gold metal

(Figure 3, stage 4).

Figure 3. Schematic representation of bioleaching (stage 1), sulfidogenic (stage 2), electrochemical

selective extraction (stage 3), and chemical extraction (stage 4) (bio)reactors.

Accelerating exhaustion of primary mineral resources has rendered secondary recourses increasingly important [35]. Mining tailings are one of the richest secondary resources often including copper, iron, zinc, and nickel in high concentrations (critical elements), and occasionally REEs, such as lanthanum, neodymium, and cerium, and precious metals such as silver and gold. Being ground in fine sizes, mine tailings are more susceptible to environmentally caused transformations. This is to the extent that mine tailings can be considered as significant polluting sources of ground/surface waters (e.g., acid and metal deposition of in Nevada to the

Owyhee River) [61]. This becomes more critical where rejects from water-treatment plants and mineral processing are deposited in the tailings. Metal value recovery from mine tailings can be carried out by conventional hydrometallurgical methods such as inorganic chemical leaching and solvent extraction. Nonetheless, these methods may require rather extreme conditions of temperature, pressure, and chemical environment.

REMARKS

Numerous studies indicate that biomining is more environmentally friendly and energy conservative. Is biomining ready to be employed with its full potential then? Despite the foregoing discussion, any premature application of biomining decelerate further developments in biomining, rather than promoting it. To avoid that, foundations of biomining must be revisited; fundamental research must be performed with respect to the multidisciplinary nature of biomining. In general terms, profitability is the major concern of engineering and not so much of science. In the field of biomining, majority of academic research (and biohydrometallurgy in general) is performed within programs other than mining and metallurgical engineering, e.g., biochemistry, microbiology, and environmental science. However, what is valuable for the market is the final product, i.e., minerals that is under the control of mining and metallurgical engineers. As far as industry is concerned, bioextraction techniques are expected to compete with traditional ones. Some of the latter techniques have been refined over thousands of years (e.g., pyrometallurgical smelting), to which investments are mainly allocated. Moreover, the slower kinetics of bioextraction introduces a substantial delay in cash flow, while technologies such as pyrometallurgical smelting benefits from higher and faster yields, justifying its higher cost.

Although biomining is considered to be more conservative about environment (as well as energy), compared to traditional mining, the negative historical impact of the mining industry on the environment has marginalized the environmentally-friendly potentials of biomining. In addition, it is hard to model and scale up biomining processes [35].

As already discussed, the lower grade of increasingly growing secondary resources compensates the slower kinetics of biomining. If the concertation of the desired elements is low, traditional mining will completely lose its privilege, and will be prevailed by biomining in all aspects; with respect to time, energy, and environment (Figure 4). For example, as an energy conservative approach, biomining can be more generous in exploring energy intensive methods, such as high- temperature bioextraction. Importantly, full potential of biomining can only be exploited/revealed if all bio-assisted stages are inclusively considered (e.g., bio-assisted pretreatment), rather than solely consideration of bioextraction stage. Moreover, it is extremely difficult to transfer millions of tons of mine waste into enclosures; therefore, practical post- treatment solutions are those which work outside in the environment where things are out of control. This requires developing a better understanding about interactions between domestic microorganisms and minerals under in-situ environmental conditions. From the analogy between biomining and algal-bacterial wastewater treatment, one can vividly see the self-regulating nature of microorganisms; there is mutual relationship between their survival and their environment. Regarding all those variables, one can optimize the operational condition of biomining as a whole within a multivariate analysis. Fortunately, within the current status of biomining, there is enough leeway to proceed bio-assisted stages in a parallel manner. Also, combining chemical processes (e.g., gangue chemistry) with biological ones (e.g., metabolic manipulation) could potentially help to reach the breaking point of profitability for low-grade ores. Eventually, biomining demands collaborations among scholars with various backgrounds due to its multidisciplinary nature. These collaborations not only lead to potential strategies to improve biomining as an industry to extract minerals but also help develop biomining (as well as the involved disciplines) as a science to understand the harmonious coexistence between minerals and microorganisms. Taken together, the more we invest on laying the bedrocks of biomining in a systematic way, the more science, technology, and environment can benefit from such foundational investment.

A dv • an E tag • ne es E rg : n y c vir on on se me rv nt ati D all ve isa y f • dv rie S an nd • low tag ly H k es ar ine : d t tic o m s od el

Figure 4. Advantages and disadvantages of biomining; the highlighted region is roughly where biomining is

more economically viable

Finally, biomining could practically benefit from analyzing life-mineral coevolution. For instance, higher diversity of copper oxide minerals has been demonstrated to favor copper in the biological structures existing in modern deposits. Similarly, higher oxidation state of manganese

(4+) is shown to be more abundant in more recent near-surface deposits, when/where life started playing a major role [2,4]. These historical analyses could also be beneficial in roughly dating the individual biological structures and estimating the conditions they have evolved in. Another possibility is to make predictions based on mineral-microorganism network analysis; where to find new minerals. Inspired by what is called “affinity analysis”, one could develop a network based on coexistence/codependency of certain mineral and microorganisms. This requires machine learning on big databases, which are rapidly being developed nowadays [3,69].

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*E-mail: [email protected] Tel: +1 618-303-7047. ORCID

Behrooz Abbasi: 0000-0003-4163-7262

Acknowledgements: Not applicable.

Authors’ contributions: All authors designed the study, and wrote, read and approved the manuscript.

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Funding Not applicable.

Data availability Not applicable.

Conflict of Interest The authors declare no competing financial interest.

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