Natural freshwater microalgae biofilm as a tool for the clean-up of water resulting from mining activities

ABSTRACT

Pollutants in aquatic environment tends to alter the community composition and activities of biofilm cells. The stress induced by these pollutants leads to the production of excessive reactive oxygen species (ROS) which play a key role in the degradation of pollutants in aquatic environment. This mini-review is aimed at forecasting the efficiency of the use of natural freshwater microalgae biofilm in the treatment of water resulting from mining activities. Moreover, it summarises the concept of mining by concisely stating the stages involved in mining and how the pollutants produced during mining can cause deleterious effects to aquatic flora and fauna. Environmental issues resulting from mining activities and how they hindered the progress of biodiversity were concisely discussed. Freshwater microalgae play an important role in the mitigation of the impact of pollution resulting from mining activities. The process of pollutants removal in freshwater by microalgae biofilm is by degradation and biosorption. However, it is an unestablished fact that the extracellular polymeric substances (EPS) were responsible for the biosorption of heavy metals from mining wastewater. It is also important to know the kinetic model that best explains the chemical and physical reactions of heavy metal absorption by the surface of microalgae biofilm.

KEYWORDS:

• Microalgae
• pollutants degradation
• mining activities
• freshwater ecosystem

Introduction

Mining is the main economic activity of many developing countries. Mining was among the major source of export in Nigeria before 1970 (Eludoyin et al. 2017). The overdependent on oil resources have intensified artisanal mining practice in the country due to lack of government will, intervention and implementation of available regulations. Mining in Nigeria is done without considering the impacts on the environment, and in most cases, reclamation is never a stage in mining process (Stewart 2020). Mining operation be it small or large scale is inherently disruptive to the environment, producing enormous quantities of waste that can have a deleterious impact for decades. The risk of pollution from mining sites lasts even after the cessation of mining activities. In all sites where mining activities exist, environmental problems are present.

These problems manifest as degradation of forest and loss of biodiversity, soil contamination, air pollution, surface and groundwater pollution, noise and vibrations, deterioration of natural drainage system, natural land degradation, negative impact on terrestrial and aquatic ecosystems, socio-economic and human health. The worsening environment caused by mining occurs mainly as a result of unsuitable and wasteful working practices and rehabilitation measures. Hence, protecting water quality is an urgent environmental challenge at mining and mineral processing sites (Ugya et al. 2018).

Many technologies have been employed in the treatment of mining wastewater, among which include desalination, clarification, evaporation and crystallization, disinfection, filtration, ion exchange, membrane separation, package plants and biological techniques (Puyol et al. 2017). These technologies are cost-ineffective and very difficult to use under field conditions, hence in such a situation, there is an urgent need to study natural, simple and cost-effective techniques for control (Guo et al. 2019). The use of natural freshwater microalgae biofilm for the clean-up of water resulting from mining activities is an alternative to conventional and other biological methods due to its cost-effectiveness, the requirement of low technological know-how and high efficiency of freshwater microalgae biofilm to remove nutrients, heavy metals, organic and inorganic wastewater from wastewater (Abdel-Raouf et al. 2012).

Natural freshwater microalgae biofilm encompasses several syntrophic groups of microorganisms in association with the inorganic surfaces. The member cells forming a freshwater biofilm become surrounded by a slimy extracellular matrix which is composed of extracellular polymeric substances (EPS) (Arunasri and Mohan 2019). The components of the EPS signify the community routine of all the member microorganism in the freshwater microalgae biofilm and have a three-dimensional structure because the EPS is produced by the accumulation of polysaccharide, proteins, lipid and deoxyribonucleic acid (DNA) of each of the members’ microorganism forming the natural freshwater microalgae biofilm (López et al. 2010).

The microorganisms developing freshwater microalgae biofilm are physiologically different from other planktonic cells of a similar organism floating in a freshwater environment (Pikoli et al. 2019). Natural biofilm consists of different types of microorganisms which could either feed autotrophically or heterotrophically. The autotrophic organisms present in natural biofilms consist of microalgae and cyanobacteria, whereas heterotrophic organisms include bacteria, fungi and protist (Xuemei et al. 2010). These organisms form a natural biofilm and accumulate on the surface of an artificial or natural substrate which are surrounded by EPS (Ugya et al. 2020). The EPS of natural biofilm is the reason why biofilm is able to resist environmental stress, thus causing the degradation of pollutants in aquatic environment (Han et al. 2017). This mini-review is thereby aimed at forecasting the efficiency of the use of natural freshwater microalgae biofilm in the treatment of water resulting from mining activities.

The concept of mining

Mining can be defined as the process by which minerals resulting from geological processes are extracted from the lithosphere (Ugya et al. 2018, Ugya et al. 2019). These economically valuable ores are a combination of different materials including metals, coal, oil shale, gemstones, limestone, chalk, dimension stone, rock salt, potash, gravel and clay (Ugya et al. 2018). The process of mining involves the extraction of non-renewable resources such as coal, crude oil, water and natural gas and is independent of material resulting from agronomic activities or materials created in the laboratory (Emmanuel et al. 2018). The unanswered question about mining operations is its negative environmental impact which has led to the creation of different laws aimed at decreasing the negative aspect of mining on the environment (Ngole-Jeme and Fantke 2017). The stages involved in mining activities include prospecting, exploration, development, exploitation and reclamation as illustrated in Figure 1.

Figure 1. The stages involved in mining activities.

The prospecting stage of modern-day mining activities is aimed at discovering and searching for valuable mineral deposits or ore. This stage is important because the minerals may be located beneath or in the surface of the earth (Alavi 2020). The methods adapted in prospecting of mining site can either be direct prospecting method or the indirect prospecting method.

The direct prospecting method is used in the exploration of valuable minerals or ores found on the surface of the earth. This method involves the use of visual examination and geologic techniques such as aerial photography, geologic mapping, structural assessment of an area and microscopic studies of sample (Griffith 1960). The indirect prospecting method is a tool that is used for the discovery of valuable ores and materials deposited beneath the earth. The indirect prospecting method used for the detection of materials is geophysical techniques including physical measurement of gravitational, seismic, magnetic, electrical, electromagnetic and radiometric variables of the earth (Day-Lewis et al. 2017).

Exploration is the second stage of mining which involves the estimation of the size and value of mineral deposits. This important stage is aimed at determining the supposed economics of the ore deposit in order to know if there is the need for further investment (Sonter et al. 2018). This stage of mining activity involves the measurement of the fiscal viability, technical and monetary danger, as well as the strength of the project. This is the stage where decision is made on continuity of the mining activity. This stage also involves the planning to evaluate the retrievable portion of the deposit (the metallurgy and ore), its economic and marketability potential, and engineering concerns, as well as an investigation of the proposed mine from the initial excavation all the way through to the recovery of land. Another issue deserving consideration is that more waste than ore is mined during the life of a mine, so waste elimination and placement are key burden to the mining operator, and as such, comprehensive characterization of the waste material formed is a crucial part of the geological exploration program for a mining operation (Considine et al. 2017). The techniques used in exploration during mining include chemical, metallurgical, X-ray, spectrographic or radiometric evaluation techniques which are meant to enhance the investigator’s knowledge of the mineral deposit (Singer and Kouda 1999).

Development is the third stage of mining activities which involves the preparation for the exploitation of mineral deposits. Before exploitation of surface mining can occur, the mineral deposits are accessed by stripping the soil or rock covering the mineral deposits while deep soil excavation techniques are used to expose the mineral deposits during sub-surface mining. The most common method of mining in Nigeria is surface mining (without petroleum and natural gas) (Obiadi et al. 2016). The developmental work that must be done before the stripping of soil/rock or the process of excavation include acquiring water and mineral rights, buying surface lands, arranging for financing, and preparing permit applications and an environmental impact statement (EIS). Other developmental work pertaining to the mining process include the provision of access roads, power sources, mineral transportation systems, mineral processing facilities, waste disposal areas, offices and other support facilities (Maier et al. 2014).

Exploitation is the fourth stage of mining involving the actual exploration of valuable minerals in quantity from the earth. This stage is initiated by the movement of mining equipment to the site and commencement of mining activities until the mineral mining is no longer economically viable (Considine et al. 2017). The two categories of materials targeted during the exploitation stage include the placer and lode deposits. The placer deposits are valuable minerals that is formed as a result of hydrologic weathering and surface weathering, e.g. alluvial, colluvial, eluvial, beach and paleo placers (Haldar 2013), while lode deposits are metalliferous ore that are found embedded in the cracks or layer of rocks (Groves and Foster 1991).

Both the placer or lode deposits are mined by both surface and underground methods. Rare earth element (cerium (Ce), dysprosium (Dy), erbium (Er), europium (Eu), gadolinium (Gd), holmium (Ho), lanthanum (La), lutetium (Lu), neodymium (Nd), praseodymium (Pr), promethium (Pm), samarium (Sm), scandium (Sc), terbium (Tb), thulium (Tm), ytterbium (Yb) and yttrium (Y)) and uranium can be mined using in-situ leaching method, which is a method that do not depend on surface or underground digging (Xie et al. 2014). The requirement for extracting target minerals by this technique is that they should be soluble, for instance, potash, potassium chloride, sodium chloride, and sodium sulfate, are soluble in water, but minerals, such as copper minerals and uranium oxide, will require acid or carbonate solutions to dissolve (Mhlongo et al. 2018).

Surface mining is performed by stripping surface vegetation, dirt, and, layers of bedrock for the purpose of getting the ore deposits. This is achieved by different methods such as open-pit method, quarrying, strip mining, and mountaintop removal. Open-pit method is the type of surface mining commonly called open cast mining, and this type of surface mining involves the extraction of valuable minerals from the borrow without the use of the tunnel because the kind of ores (sand, cinder and gravel) extracted using this method are always near the surface (Zendehboudi and Bahadori 2017). Quarrying is similar to open-pit mining but it deals with sand, stone and clay. Strip mining is a type of surface mining usually called the overburden removal that is used for the mining of coal and lignite.

This mining technique involves the removal of long strip of overlying soil or rock covering the ore/seams underneath (Cole 1999). The mountaintop removal is a type of surface coal mining technique that occurs at the summit ridge of a mountain (Hendryx et al. 2019). The final stage of mining activities is reclamation which involves the recontouring, revegetation and restoring of water and land values. The process of restoration should begin after the excavation process is initiated (Ezeokoli et al. 2020). Since the concern of mining industry is to maintain sustainability, it is important to address some issues during reclamation in order to sustain the economic and environmental needs of the present and future generation (Virgone et al. 2018). These issues include safety of mine site, restoration of land surface and water and change of land use after mining (Virgone et al. 2018).

Environmental issues resulting from mining activities

Environmental issues resulting from mining activities are as a result of the direct or indirect impact of mining practices. These issues are of local, regional and global concern and arose from the emission during mining activities (Navarro et al. 2004). These emissions led to environmental issues such as sinkholes, erosion, soil contamination, water contamination (surface and ground water) (Figure 2), loss of biodiversity and deterioration of air quality (Haddaway et al. 2019). The process of mining is associated with soil degradation and erosion leading to the destruction of large area of land. Erosion and degradation are as a result of mining activities such as open pit and overburden mining, construction, etc. (Ćwieląg-Drabek et al. 2020). Soil degradation is as a result of the contamination of soil by the chemical pollutants produced during mining activities (Eludoyin et al. 2017). One major effect of soil erosion resulting from mining activities is the link with water resources contamination, sinkhole and decline in biodiversity (Harfoot et al. 2018). The pollutants produced during mining activities can seep into aquifers and pollute underground water or erode into nearby surface water leading to increase in pollution, stream sedimentation, clogging of water ways and loss of biodiversity (Tarras-Wahlberg et al. 2001). During mining activities such as blasting, excavation and transportation, particulate and gases matter are dispersed by wind to the atmosphere causing air pollution (Yu et al. 2017). This air pollution tends to affect human health, global climate and the environment (water, soil and wildlife) (Almalki 2019).

Figure 2. Impact of mining activities on surface and ground water (MINEO consortium, 2000).

The impact of mining activities on biodiversity

The modification of habitat resulting from mining activities is associated with disturbance and persistence adverse health effects on both aquatic and terrestrial organisms (Taylor-Brown et al. 2019). Damaging of the original site is more detrimental to biodiversity because the pollutants produced during mining activities are toxic and can directly or indirectly affect biodiversity (Prach and Tolvanen 2016).

The modification of the habitat is associated with change in pH and temperature which in turn causes disturbances to the surrounding community. Cosmopolitan species are likely to adapt to the change in pH and temperature while endemic species are negatively affected due to slight variation in the condition of their habitat which increase the risk of extinction (Davidson et al. 2017).

The mobility and bioavailability of pollutants produced during mining activities determine the effect of the pollutants on biodiversity (Wuana and Okieimen 2011). The less-mobile pollutants remain in the mining site, whereas highly mobile pollutants move into nearby environment or are been taken up by organism (Sharma and Bhattacharya 2017).

Some pollutants produced during mining activities tend to be bioavailable while others evolve in the environment. This difference in bioavailability led to variation in the level of toxicity to organisms (Tchounwou et al. 2012). The ability of some pollutants (heavy metals) produced during mining activities to bioaccumulate also determines the effect of these pollutants on biodiversity. This is because heavy metals tend to bioaccumulate across the food chain to the level that it causes toxic effects to organisms. On the other hand, contaminants that do not bioaccumulate tend to degrade and completely disappear from the contaminated zone especially with low concentration (Jain and Das 2017).

Impact of mining activities on aquatic organisms

Aquatic biodiversity is impacted by mining in different ways. One of which is direct poisoning; this happens when contaminants are bioavailable in the water and/or freely mobile in the sediment. Contaminants can physically affect aquatic organisms. Example including high concentrations of suspended sediment in a stream tends to limit penetration of light which may diminish algal biomass. Metal oxide deposition limits biomass by coating algae or their substrate, thus preventing colonization. Also, temperature, rainfall, pH, salinity and metal concentrations in a stream can in the long run affect aquatic communities. pH or temperature changes affect metal solubility making it more bioavailable for uptake by organisms.

It is noteworthy that metal contaminants persist in the habitat for a very long time up to 90 years after pyrite mine closure. Mine drainages cause distress in algal communities leading to decreased primary productivity. Both physical and chemical changes in aquatic environment tend to affect diatoms population. In the extreme, the diatom population may become extinct. Some macroinvertebrates like aquatic insect and crustacean communities are altered due to mining resulting in a low trophic completeness and may become unbalanced with predators dominating their community. Macroinvertebrate diversity may persist if sensitive species are replaced with tolerant ones (Huang et al. 2010).

Pollution in freshwater environment resulting from mining activities

The pollutants produced during mining activities are in the form of organic and inorganic. Biological pollutants are divided into two classes based on polarity as hydrophilic and hydrophobic organic pollutants (Schweitzer and Noblet 2018). The polar organic contaminant that is soluble in water is referred to as hydrophilic pollutants while the non-polar and insoluble organic contaminant is known as hydrophobic organic contaminant (Nanny and Ratasuk 2002). Hydrophilic contaminants are organic pollutants that do not readily affect freshwater ecosystem owing to their non-persistence nature and ability to dissolve in water, common example of hydrophilic contaminant includes organic pollutants with relatively small alkyl group such as alcohol and carboxylic acids (CH₃, C₂H₅, C₃H₇ and C₄H₅). Another important example is methyl tertiary butyl ether (MTBE) (Qin et al. 2010). Hydrophobic contaminants are the most worrisome organic contaminants due to their persistence’s nature and inability to dissolve in water, example of these pollutants includes dichlorodiphenyltrichloroethane (DDT), polychlorinated biphenyls (PCBs), polybrominated diphenyl ethers (PBDEs), polychlorinated dibenzodioxins (PCDDs), polychlorinated dibenzofurans (PCDFs), polyaromatic hydrocarbons (PAHs), benzene toluene, ethylbenzene and xylene (BTEX) (Jaffé 1991) (Table 1). Inorganic pollutants include heavy metals, phosphorus compounds, nitrogen compounds, halide compound, sulphide compounds, etc. (Baykoucheva 2015) (Table 1). Heavy metals are the most persistent inorganic contaminants due to their non-biodegradable capacity (Tchounwou et al. 2012). Nevertheless, these elements might be found in a very low concentration in the environment but they tend to be detrimental to aquatic flora and fauna due to their ability to bioaccumulate along the food chain. Phosphorus and nitrogen containing compounds are also worrisome in the environment due to their contribution in eutrophication which leads to the growth of harmful algae (Heisler et al. 2008).

Table 1. The effect of organic and inorganic contaminant resulting from mining activities.

S/N	Type of pollutant	Class of contaminant	Environmental effect of contaminant	References
1	DDT	Organic	It tends to accumulate in sediment, water and organisms of freshwater habitat, it affects the diversity of fungi, bacteria and protist. it is reported to cause reproductive failure in fishes and aquatic birds that prey on fishes	Ghani et al. (2009)
2	PCBs	Organic	Accumulate in sediment, water and organisms of freshwater habitat, is reported to cause reproductive failure in fishes and aquatic birds that prey on fishes	Cui et al. (2020)
3	PBDEs	Organic	Accumulate in sediment, water and organisms of freshwater habitat, is reported to cause reproductive failure in fishes and aquatic birds that prey on fishes	Liu et al. (2018)
4	PCDDs	Organic	Accumulate in sediment, water and organisms of freshwater habitat, is reported to cause reproductive failure in fishes and aquatic birds that prey on fishes	Kannan et al. (2008)
5	PCDFs	Organic	Accumulate in sediment, water and organisms of freshwater habitat, is reported to cause reproductive failure in fishes and aquatic birds that prey on fishes	Chen et al. (2012)
6	PAHs	Organic	PAH is utilized by aquatic organisms including mollusks, crustaceans, polychaetes, fish etc., but at higher concentration PAH tend to be toxic to marine organisms leading to reproductive and endocrine failure in fish	Brewster et al. (2017)
7	BTEX	Organic	BTEX are moderately toxic to aquatic flora and fauna at higher concentration which resulted from spillage but are unlikely to cause any toxicity at normal environmental level because they degrade easily.	(Fernandes et al. 2014)
8	Ammonia	Inorganic	Causes Eutrophication and algae blooms	Sonthiphand et al. (2013)
9	Nitrate	Inorganic	Causes Eutrophication and algae blooms	Li et al. (2013)
10	Phosphate	Inorganic	Causes Eutrophication and algae blooms	Wang and Liang (2015)
11	Heavy Metals	Inorganic	Effect depend on the type of heavy metal but toxicity of all heavy metal in freshwater organisms results when the uptake rate exceeds the combined standards of detoxification	Duncan et al. (2018)

Source: Modified from Ajibade et al. (2020).

Harmful microalgae can be very dangerous to freshwater habitat due to the formation of algae blooms (Mohamed 2018). Microalgae blooms vary in colour from green, yellow or brown colour depending on the species of microalgae involved (Wells et al. 2015). This bloom is caused as a result of excessive utilization of nutrients by harmful microalgae particularly in slow moving water bodies such as lake and ponds (Mohamed 2018).

This bloom produced by freshwater microalgae is extremely toxic to freshwater biota because they tend to block the gills of fishes and other freshwater micro invertebrate and also depletes the available dissolve oxygen in freshwater habitat leading to the death of freshwater organisms (Schmale et al. 2019).

Blooms can also make an ecosystem to be unsustainable because they tend to be poisonous to the smaller fishes and other filter feeder organisms that feed on them and this toxicity can move across the food web resulting into the death of macro plants in freshwater environment (Paerl 2018).

Harmful microalgae can also affect aquatic productivity because they prevent sunlight energy from penetrating deep into other freshwater zones leading to the reduction in the diversity of organisms in the freshwater habitat (Heisler et al. 2008). The prevention of sunlight by harmful microalgae could be based on the decolouration of freshwater habitat by harmful microalgae or due to the formation of thick film on the surface of freshwater by freshwater microalgae (Wang et al. 2017).

Harmful microalgae bloom also affects the mobility of freshwater fauna such as coral and can also affect other freshwater flora from having access to sunlight for photosynthesis because they submerged this freshwater flora and also serve as a shade, thereby preventing sunlight energy from reaching the organisms. Harmful microalgae are able to produce micro toxins that have detrimental effects on freshwater biota particularly fishes and other micro- and macroinvertebrates (Stauffer et al. 2019).

Formation and composition of natural freshwater microalgae biofilm

Freshwater microalgae are microorganisms that are adapted to freshwater environment. They are unicellular and free living organism that ranges in size from 4 to 178 µm (Ugya et al. 2020). Microalgae are able to utilize light, carbon dioxide and water for the process of photosynthesis to generate the energy needed for metabolic activities. The growth of microalgae also depends on major nutrients such as nitrogen and phosphorus (Zullaikah 2019).

Natural freshwater microalgae biofilm is formed by the attachment of free-floating microalgae to organic or inorganic substrate (Donlan 2002). The initial freshwater microalgae that form the biofilm are able to attach to the substrate at first by the help of weak Van der Waals force of attraction and hydrophobic effect before being attached permanently with increasing density of the freshwater microalgae (Davey and O'Toole 2000). The process of biofilm formation by freshwater microalgae can be divided into five stages. The stages of freshwater microalgae biofilm formation include initial attachment, permanent attachment, initial maturation, permanent maturation and dispersion (Muhammad 2020).

The stages of natural freshwater biofilm represented in Figure 3 depict that during the initial and permanent attachment stages, the EPS was not formed due to the visibility of the substrate, though the number of freshwater microalgae on the substrate during the initial attachment stage is fewer than the permanent attachment stage (Miranda et al. 2017). The EPS was formed during the initial maturation, permanent maturation and dispersion stage, despite the thickness of the natural freshwater biofilm of the permanent maturation and dispersion stages is thicker than the initial maturation stage (Roostaei et al. 2018). The reason why higher biomass of the freshwater microalgae were found during the maturation and dispersion stages when compared to the attachment stage is owing to the fact that during the attachment stage, some freshwater microalgae were not able to anchor to a substrate instead it attached to the EPS during the maturation and dispersion stages (Roostaei et al. 2018). The dispersion stage is the final stage of freshwater biofilm microalgae formation and is the stage in which the freshwater microalgae biofilm is established and may undergo alteration in form and size. Enzymes such as dispersin B and deoxyribonuclease play important role in the dispersal of freshwater microalgae biofilm because they have the ability to degrade the EPS (López et al. 2010).

Figure 3. The process of natural freshwater microalgae biofilm formation (a) initial attachment (b) permanent attachment (c) initial maturation (d) permanent maturation (e) dispersion.

Freshwater microalgae biofilms are usually found naturally on solid substrates submerged in aquatic environment, although they can sometimes form a floating mat on the surfaces of aquatic habitat. Microalgae biofilm often grow to macroscopic level but tend to contain diverse kinds of microorganisms including bacteria, archaea, protozoa and fungi with each group of organism playing a particular metabolic role (Besemer 2015).

Factors influencing natural microalgae biofilm formation

There are no much information on the factors that influences the formation and structure of natural freshwater microalgae biofilms, this is because the formation of natural freshwater microalgae biofilm is depended on different parameters and interactions among the microbes involved in the biofilm formation (Mantzorou and Ververidis 2019). In order to determine the mechanism involved in the regulation of pollutants in natural environment by freshwater natural biofilm, it is crucial to know the most influential parameter for the formation of natural freshwater microalgae biofilm (López and Soto 2019). This mini-review is structured specifically to consider the role of nutrients, light intensity, temperature, pH, inorganic carbon, the role of other microbes, growth substrate, water flow and nature of EPS formed. This mini-review will not consider the selection of microalgae strain as part of the factors that influences the formation of natural microalgae biofilm because the study is aimed at a natural system where the ecological significance is dependent on the structure of microbe forming the biofilm, as such, it is paramount to determine the community of microalgae forming the biofilm using relevant microbiological and molecular techniques (Rutherford and Bassler 2012).

Nutrient availability

Fresh water microalgae utilized the nutrients such as nitrate and phosphorus present in aquatic environment for natural biofilm formation (Delgadillo-Mirquez 2016). Although, it is a well-established fact that during the early growth stage of freshwater microalgae, the cells are metabolically active and tend to utilize more nutrient than the late growth stage when the cell is less active metabolically (Moreno Osorio et al. 2019).

This principle tends to be insignificant for natural freshwater biofilm formation because at the early growth stage, the biofilm is not yet settled based on its low density and absence of EPS, thereby using up lesser amount of nutrients compared to that at the late growth stage when the microalgae is fully matured, which has higher density and settle comfortably on the organic substrate (Zhu et al. 2016). The formation of EPS also contributes to the high usability of nutrient because the EPS aids the attachment of other non-microalgae organism which also need nutrient to survive (Pierre et al. 2019). Studies have shown that elevated nutrients concentration in aquatic environment tends to promote EPS production while nutrient starvation leads to the degradation of EPS resulting to the detachment of the contributing organism in the biofilm formation (Kesaano and Sims 2014).

The large amount of nutrient used up by the freshwater microalgae biofilm at the late stage of formation is the reason why the biomass of freshwater microalgae cannot be used for lipid production. Furthermore, it buttresses the reason why any aquatic bodies consisting of freshwater microalgae biofilm do not permit algae blooms (Zhu et al. 2016).

Availability and duration of light

Natural freshwater biofilm depends on light for formation, because freshwater microalgae are autotrophic organisms that rely on light for the production of food via photosynthesis and also EPS production (Pierre et al. 2019). The availability and duration of light tend to play a significant role in the formation of freshwater microalgae biofilm in natural environment (Shen 2014). This presence of light led to the increase in nutrient utilization, thus enhancing the production of EPS which in turn attracts more organisms into the biofilm (Moreno Osorio et al. 2019). Whereas the increase in duration of light could be detrimental to the freshwater microalgae formation because the freshwater microalgae could undergo oxidative stress (Diaz and Plummer 2018), consequently, affecting the formation of the biofilm. Moreover, this can be attributed to the reason why some freshwater environment never form natural freshwater microalgae but rather algae blooms (López et al. 2010).

Natural freshwater microalgae biofilm extracellular matrix (EPS)

The EPS matrix of freshwater microalgae is a three-dimensional network consisting of exopolysaccharides, proteins and nucleic acids that gives biochemical and structural supports to the cells (that make up the freshwater biofilm) (López et al. 2010). The role of the EPS in the biofilm association is to encase the cells and also aid in the communications, biochemical signals and gene exchange (Costa et al. 2018). The EPS also plays a role in the external digestion of pollutants because the matrix traps extracellular enzymes and keep them in close proximity to the participant cells (Decho and Gutierrez 2017). Freshwater biofilms contain water channels that help in the distribution of nutrients and signalling molecules (Decho and Gutierrez 2017).

Freshwater microalgae in a biofilm association are likely to possess different characteristics to free-floating freshwater microalgae by reason of the interaction occurring between the freshwater microalgae and organisms within the dense and protected environment of the film. The reason why freshwater microalgae are highly resistant to detergents and antibiotics is because the dense extracellular matrix and the outer layer of cells protect the interior of the community (Stoodley et al. 2002).

The role of natural freshwater microalgae biofilm in pollutant degradation from mining wastewater

Mining activities is associated with the production of wastewater which is detrimental to the flora and fauna of freshwater environment. The utilization of freshwater microalgae biofilm in the treatment of mining wastewater will help to minimize the menace associated with the production of this wastewater due to the natural principle behind the production of freshwater microalgae biofilm, making it easily accessible and cost effective (Escapa et al. 2017).

The mechanisms involved in pollutant degradation by microalgae biofilm are a natural process involving biosorption and interaction. Since thousands of microalgae cell are involved in microalgae biofilm formation, these biofilm can biodegrade or biotransform pollutants resulting from mining activities by either degradation or accumulation (Wang et al. 2019). The ability of microalgae biofilm to cause the degradation of pollutants present in mining wastewater could be as a result of the enzyme activities produced by the individual microalgae cell present in the biofilm (Baghour 2019) or due to the increased level of reactive oxygen species (ROS) produced as a result of the high amount of microalgae cells forming the biofilm (Ugya et al. 2020).

Many studies have shown that freshwater microalgae biofilm is able to produce reactive oxygen species (ROS) which is capable of oxidizing persistent organic compound, thereby bringing about the degradation of these compounds into CO₂, CO₃^2- and H₂O with the products being utilized by the freshwater microalgae for biomass production (Shi and Xu 2019). Studies by Ugya et al. (2020) show that freshwater microalgae biofilm is able to produce ROS of high concentration, which is capable of degrading persistent organic compounds such as trichlorobenzene, tetrachlorobenzene, alkyl halides, and some heavy organic compounds such as PCBs. These studies also reveal that the ROS produced by freshwater microalgae is capable of degrading sulphur containing pollutants because of the potentiality of ROS to desulfurize thiocarbonyl compounds such as thiouracils, thioamides and thioureas to carbonyl compounds (Shi and Xu 2019).

Freshwater microalgae have cellular organization similar to bacteria but also different in their ability to perform photosynthesis. The ability of freshwater microalgae to perform photosynthesis is very important to life on water and land because during the photosynthetic process, they are most likely to exhaust the greenhouse gases particularly CO₂ produced during mining activities leading to the production and release of more oxygen (Benedetti et al. 2018).

Microalgae biofilm is able to remove inorganic substances such as phosphorus, ammonia and nitrogen compounds present in freshwater habitat by utilizing these substances for biomass production, thereby preventing the substance from accumulating to a toxic level in freshwater habitat (Naidoo 2019).

Freshwater microalgae are also able to oxidize or reduce toxic metals in freshwater environment, thus preventing the toxicity to freshwater biota (Cakmak et al. 1987). This is also possible via the production and release of ROS by freshwater microalgae which oxidized these toxic metals to usable elements by the freshwater microalgae. Studies by Cakmak et al. (1987) in marine environment show that the ROS produced by marine microalgae is capable of increasing the amount of iron present in the environment via the reduction of ferric compounds (Cakmak et al. 1987).

Conclusion and future direction

Mining activities negatively alter both aquatic and terrestrial ecosystems in enormous ways. The water generated tend to affect the biota of the receiving surface water and also pose a critical threat to the public health of terrestrial organism. The incessant artisanal mining activities in developing countries are worrisome due to the menace associated with it. Most artisanal mining is carried out without environmental impact assessment (EIA), and as a result, the fate of the environmental pollutants produced during mining activities is not considered. These unofficial mining activities are the rationale behind lead poisoning in three local government areas of Zamfara State in Nigeria, which was recorded in March 2010 (Udiba et al. 2019).

Microalgae biofilm can effectively be used as a tool in the remediation of water pollution resulting from mining activities. This is because microalgae biofilm can occur naturally in aquatic environment, so its usage under field conditions will never be a difficult task. The enhancement of environmental factors such as nutrients and light will help freshwater microalgae biofilm formation. Microalgae biofilm tends to prevent the occurrences of algae blooms which is the severe threat to freshwater environment. The stimulations of environmental factors can also make freshwater microalgae biofilm to release higher amount of reactive oxygen species (ROS) that can regulate the growth of bacteria, thereby minimizing the loss of dissolved oxygen (Udiba et al. 2019).

Although, microalgae biofilm removes pollutants from mining wastewater by degradation and biosorption. More research needs are required to clarify if the enzymes released by microalgae biofilm during degradation process are the sole obligation of the entire cells partaking in the biofilm or that of the extracellular matrix. There is also a need to explore the role of EPS in the biosorption process of heavy metal removal from mining wastewater and explain its removal mechanism. It is also important to comprehensively understand the kinetic model that best explains the chemical and physical reactions of heavy metal absorption by the surface of microalgae biofilm.

Acknowledgment

The first author appreciates the support rendered by the PTDF 2018 PhD scholars of Jilin University Changchun, China

Disclosure statement

No potential conflict of interest was reported by the authors.

Additional information

Funding

This work was supported by Natural Science Foundation of Jilin Province: [Grant Number 20170101079JC]; Petroleum Technology Development Fund: [Grant Number PTDF/ED/PHD/APY/54/18]; National Natural Sciences Foundation of China: [Grant Number 42077343].