Available online at www.sciencedirect.com Plant based phosphorus recovery from wastewater via algae and macrophytes Andrew N Shilton, Nicola Powell and Benoit Guieysse At present, resource recovery by irrigation of wastewater to plants is usually driven by the value of the water resource rather than phosphorus recovery. Expanded irrigation for increased phosphorus recovery may be expected as the scarcity and price of phosphorus increases, but providing the necessary treatment, storage and conveyance comes at significant expense. An alternative to taking the wastewater to the plants is instead to take the plants to the wastewater. Algal ponds and macrophyte wetlands are already in widespread use for wastewater treatment and if harvested, would require less than one-tenth of the area to recover phosphorus compared to terrestrial crops/pastures. This area could be further decreased if the phosphorus content of the macrophytes and algae biomass was tripled from 1% to 3% via luxury uptake. While this and many other opportunities for plant based recovery of phosphorus exist, e.g. offshore cultivation, much of this technology development is still in its infancy. Research that enhances our understanding of how to maximise phosphorus uptake and harvest yields; and further add value to the biomass for reuse would see the recovery of phosphorus via plants become an important solution in the future. Address School of Engineering and Advanced Technology, Massey University, Private Bag 11-222, Palmerston North, New Zealand Corresponding author: Shilton, Andrew N ([email protected]) Current Opinion in Biotechnology 2012, 23:884–889 This review comes from a themed issue on Phosphorus biotechnology As phosphorus becomes increasingly scarce, it would seem likely that irrigation specifically for the purpose of phosphorus recovery will increase. However, this can be far more challenging than it initially appears due to: 1. Quality constraints requiring treatment: dependant on the type of crop irrigated (and its subsequent use) and the wastewater source, additional treatment stages may be required to mitigate risks due to pathogens and/or toxins. 2. Temporal constraints requiring storage: crops have a seasonally variable demand for phosphorus and water. In arid regions large storage reservoirs are required to match irrigation to the dry season, whereas in other regions reservoir storage is required during wet seasons to prevent leaching to groundwater and/or runoff to surface waterways [4,5]. 3. Spatial constraints requiring conveyance: a. In some agricultural regions where intense farming uses imported stock feed the waste needs to be conveyed back out of the district due to tight restrictions to avoid localised phosphorus overloading of soils [6]. b. Conversely, for phosphorus in domestic wastewater the challenge is the large quantity of very dilute wastewater. For example, to move 1 kg of phosphorus requires the transport of approximately 150,000 kg of domestic wastewater. Furthermore, the larger the population the wastewater is derived from, the longer the distance the reticulation system is to reach suitable agricultural land. Edited by Andrew N Shilton and Lars M Blank For a complete overview see the Issue and the Editorial Available online 10th August 2012 0958-1669/$ – see front matter, # 2012 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.copbio.2012.07.002 Introduction Irrigation of wastewater back to crops or pasture seems an obvious solution for closing the phosphorus cycle. While often feasible for agricultural wastes, it is less common for domestic wastewater. In countries such as Israel [1], West Africa [2] and Australia [3] irrigation of domestic wastewater is driven by the value of the water resource rather than the nutrient value; however, as a consequence of this practice phosphorus is also recovered. Current Opinion in Biotechnology 2012, 23:884–889 Providing treatment, storage and conveyance to address the above constraints comes at significant expense. When water scarcity is not the key driver for implementing irrigation to crops or pasture then, as illustrated in Figure 1, an alternative is to use an intermediate stage that effectively concentrates the dilute, dissolved phosphorus into a solid biomass for reuse. There are a number of treatment options for concentrating dissolved phosphorus from the wastewater into a solid including the use of adsorptive filters, precipitation reactions and bacterial uptake (in particular the enhanced biological phosphorus removal activated sludge process, EBPR). These options are covered by other reviews [7,8] written as part of this journal issue on phosphorus. However, there is also an alternative to ‘taking the wastewater to the plants’ by instead ‘taking the plants to the wastewater’ [9]. Algae and macrophytes, which can recover www.sciencedirect.com Plant based phosphorus recovery from wastewater Shilton, Powell and Guieysse 885 SOURCE Figure 1 Wastewater (domestic, industrial, agricultural) IRRIGATION EBPR Physical/ chemical Focus of other reviews in this journal issue [7,8] REUSE Harvesting Application to terrestrial crops Use as an animal feed CONCENTRATION Plants (algae/macrophytes) Value added products Current Opinion in Biotechnology Overview of options to utilise plants to recover phosphorus from wastewater. phosphorus in less than one-tenth of the land area required by terrestrial crops (see Box 1), are already widely used for wastewater treatment around the world and are reviewed in the following sections. Phosphorus recovery by algae Algae are ubiquitously used for wastewater treatment in facultative and high rate aerobic ponds around the world because of their ability to facilitate cost effective treatment of organic carbon and pathogenic pollutants [10,11]. Unfortunately, phosphorus removal is variable and most commonly quite low in these systems [12,13]. In facultative ponds algal assimilation is not capable of removing all the phosphorus found in the wastewater as these ponds are not designed to optimise biomass productivity. There is, however, potential for using high rate algal ponds which have higher biomass productivity as they are shallow, gently mixed and operated at relatively short retention times. Furthermore, as reported by Richmond [14] the phosphate content of algal dry biomass could reach up to 3.3%, which is considerably higher than the 1% content typically achieved in ‘normal’ pond algal biomass. This finding was recently confirmed by Powell et al. [15] who showed that the phosphate content of a mixed algal continuous culture grown on synthetic wastewater in the laboratory could be varied between 0.41 and 3.16% depending on the conditions they were exposed to. The extent of this ‘extra’ storage, accumulated in the form of polyphosphate, is a function of the light intensity, www.sciencedirect.com the phosphate concentration in the medium, and the temperature [16,17,18]. While research has not yet attempted to maximise phosphorus accumulation at full scale, maintaining a 3% phosphorus concentration could potentially reduce the area requirement for phosphorus uptake from a high rate pond to just 5–6 m2/capita (Box 1) and reduce costs for harvesting, transporting and spreading the biomass as a fertiliser by over 60% compared to algae with a ‘standard’ phosphorus content. Both biomass growth and harvesting must be maximised in order to maximise phosphorus recovery. At present the number of treatment ponds with algal harvesting is very limited. High rate algal ponds have a higher biomass concentration than other pond designs and are dominated by non-motile algae which helps facilitate simple gravity harvesting of the algal biomass. Furthermore, Park et al. [19] found that their harvesting efficiency could be enhanced from 60% to >85% when a proportion of the biomass was recycled. While the vast majority of full scale, algal based wastewater treatment systems involve suspended algae there has also been interest in immobilisation of algae in beads and ‘algal turf scrubbers’ [20,21]. Algae can be entrapped into beads made of materials such as alginate, carrageenan and chitosan to assimilate phosphorus. Phosphorus adsorption or precipitation also occurs on the media used to immobilise the cells. Fierro et al. [22] found that immobilised Scenedesmus achieved 94% phosphorus Current Opinion in Biotechnology 2012, 23:884–889 886 Phosphorus biotechnology removal compared to the control without algae which achieved 60%. Algal turf scrubbers are an attached growth technology where an algal biofilm is grown on a surface and so is easily harvested by scrappers. This technique has been used for treating many types of wastewater including dairy [9] and swine manure [23]. As we look out to a phosphate scarce future, algal based phosphorus recovery could significantly expand offshore. Around the world there are massive discharges of wastewater directly to seas and oceans. Thus installation of booms to form offshore floating pond systems around the naturally buoyant discharges from wastewater outfalls has been proposed [24]. Optimising for algal growth and harvesting from offshore systems may even present superior economics to ‘on shore’ algal cultivation due to the absence of the highly significant land cost component. Phosphate recovery by macrophytes Shifting to larger aquatic plant species, floating macrophytes such as water hyacinth (Eichhornia crassipes) and duckweed (Lemnaceae minor) grow on the surface of ponds whereas emergent macrophytes are grown in what are commonly referred to as constructed wetlands. Most common is the use of emergent macrophytes. These plants are adapted to grow up through the water column with their root zone and stems submerged. A recent innovation is the development of emergent macrophyte species supported by a floating mat so that the long roots of these plants grow through the mat and down into the water column providing a large surface area for biofilm development [25,26]. Because the roots in these new systems are kept suspended in the water column, all nutrient requirements for the plants must be extracted from the wastewater rather than the soil/media into which they are normally planted in conventional constructed wetlands [25]. Some researchers state that phosphorus removal in wastewater wetlands is predominantly due to biomass growth [27]. Others note that there is the potential for achieving luxury uptake in macrophytes with phosphorus contents of up to 2.9% being reported [28,29]. It has also been found that the contribution made by biofilms growing on the plants can be significant and has been reported to account for up to 31–71% of phosphorus removal. Xu and Shen [30] described a duckweed-based system which retained a high phosphate removal in winter despite limited duckweed growth and attributed this to improved protein accumulation by the duckweed and nutrient uptake by attached biofilm of algae and bacteria. While plants provide nutrient storage during the growing season, at present the plants are seldom harvested from wastewater treatment wetlands and so the nutrients are re-released when the plant material is left to decay [31]. Indeed, most of the recent research related to phosphorus removal in wetland treatment systems instead focuses on the adsorption–precipitation reactions of phosphate with Box 1 How much area is required to recover phosphorus via plants? The area required by plants to recover phosphorus is dependent on their % phosphorus content and their areal biomass productivity. Taking typical values of domestic wastewater phosphate content of 3.6 gP/person-day, approximate comparisons of the area of plants required to uptake the phosphorus from domestic wastewater on a per capita basis can be made as seen below. The comparative biomass yields are indicative only as growing conditions such as irradiance and temperature are not exactly matched. Switchgrass and maize are included as examples of relatively high yielding terrestrial crops (both commonly proposed for bioenergy production). It could be generalised that, if harvested, macrophytes and algae would require less than one-tenth of the area to recover phosphorus compared to terrestrial crops/pastures. The required area could be further decreased if the phosphorus content of the macrophytes and algae biomass was tripled from 1% to 3% via luxury uptake. Area (m2/person) Biomass yield tonne/ha yr %P per dry weight Switchgrass 8.7–12.9 [35] 0.3% [40] Maize 9–30 [36] 0.3% [40] Macrophytes 35–106 [37,38] 1% [28,29] 12-38 Macrophytes (high %P) 35–106 [37,38] 3% [28,29] 5-13 Algae 69–91 [39] 1% [14] 14-19 Algae (high %P) 69–91 [39] 3% [15] 5-6 340-503 340-503 146-487 146-487 Notes: The boxes are drawn schematically, they are not to scale. In the algal and macrophyte systems, phosphorus would also been assimilated by heterotrophic bacteria which would further increase the P uptake. Current Opinion in Biotechnology 2012, 23:884–889 www.sciencedirect.com Plant based phosphorus recovery from wastewater Shilton, Powell and Guieysse 887 the supporting physical media the macrophytes are planted into [32–34], rather than plant uptake per se. However, looking to the future it is notable that a key advantage of recovering phosphorus using floating macrophytes and, potentially floating mat emergent systems, is that the harvesting of the biomass may be easier to facilitate than that of suspended microalgae. grown rather than the mixed cultures typically found in wastewater treatment systems. Interestingly, plant biomass even has found application as a physicochemical absorbent with Chen et al. [50] investigating water hyacinth as an absorbent filter system for phosphate recovery. Conclusions Reuse As indicated in Figure 1, the algal/macrophyte biomass grown to recover phosphorus from wastewater can be utilised in several ways such as for a fertiliser or as a food source in its own right. In order for this biomass to replace traditional phosphorus fertilisers the harvesting, transportation, stability, application techniques and the proportion of phosphorus availability to crops must be considered. Unlike bacterial biomass from ‘enhanced biological phosphorus removal’ systems which quickly re-releases stored phosphorus under anaerobic conditions, Powell et al. [41] showed that algal biomass can retain stored phosphorus for some days. Furthermore, with regard to its fertiliser potential, Mulbry et al. [42] compared seedling growth using dried algal biomass to commercial fertiliser and showed growth at comparable levels. However, overall these issues from harvest to application are currently quite poorly covered by the literature for both algae and macrophytes. Algae have been identified as making a good supplementary livestock feed, such as for chickens, due to their high protein content [43,44]. Macrophytes from wetland treatment systems have been used as cattle feed [45] and there is interest in use of emergent wetland plants with higher feed value such as Taro [46]. Plants can be used as a food source for a range of aquatic animals including fish, molluscs and shrimps [44]. With careful management, to minimise any risk of contamination, aquaculture ponds can be successfully used at the end of algal pond systems transforming the plant biomass into fish biomass which is easily harvested [47]. As the value of phosphorus increases we would expect to see an increasing move to a ‘cascade’ of phosphorus recovery where the phosphorus discharged from one process is used for the cultivation of a following stage. For example, Endut et al. [48] reported on the further downstream treatment of aquaculture effluent via hydroponic cultivation of water spinach and mustard greens. Plant biomass also has the potential to be used in other value added products such as human food supplements, cosmetics and extraction of high value cellular components [49] all of which applications represent a saving of mined phosphorus resources. However, these more specialised products generally require specific strains of algae to be www.sciencedirect.com Domestic wastewater irrigation is currently more driven by the value of the water resource rather than phosphorus recovery. While irrigation can be expanded for increased phosphorus recovery, providing the necessary treatment, storage and conveyance comes at significant expense. An alternative to taking the wastewater to the plants is to instead take the plants to the wastewater. Algal ponds and macrophyte wetlands are already in widespread use for wastewater treatment and if harvested, require less than one-tenth of the area to recover phosphorus compared to terrestrial crops/pastures. This area could be further decreased if the phosphorus content in the macrophytes and algae biomass was tripled from 1% to 3% via luxury uptake. Multiple technology options exist for cultivating algae and macrophytes including immobilisation of algae in beads, algal turf scrubbers, offshore cultivation systems and floating wetland mat systems as well as new approaches for optimising harvesting, e.g. incorporating recycle so as to improve gravity settling of algae. However, research into alternative cultivation methods and reuse of the biomass as a fertiliser or stock food are still in their infancy. Further research, particularly at field scale, that enhances our understanding of how to maximise the phosphorus content of the biomass, improve efficiency of cultivation and harvesting, and add value to the biomass for reuse would see the recovery of phosphorus via plants become an important solution in the future. References and recommended reading Papers of particular interest, published within the period of review, have been highlighted as: of special interest of outstanding interest 1. Brenner A: Limitations and challenges of wastewater resuse in Israel. Clean Soil and Safe Water, NATO Science for Peace and Security Series C: Environmental Security, Part 1. 2012:3-9. 2. Akponikpe PBI, Wima K, Yacouba H, Mermoud A: Reuse of domestic wastewater treated in macrophyte ponds to irrigate tomato and eggplant in semi-arid West-Africa: benefits and risks. Agric Water Manage 2011, 98:834-840. 3. Barker F, Faggian R, Hamilton AJ: A history of wastewater irrigation in Melbourne, Australia. 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