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waterArticleBiomass Production and Removal of Nitrogen and Phosphorusfrom Processed Municipal Wastewater by Salix schwerinii:A Field TrialMuhammad Mohsin 1, * , Erik Kaipiainen 1 , Mir Md Abdus Salam 1,2 , Nikolai Evstishenkov 1 , Nicole Nawrot 3 ,Aki Villa 1 , Ewa Wojciechowska 3 , Suvi Kuittinen 1 and Ari Pappinen 1, *123* Citation: Mohsin, M.; Kaipiainen, E.;Salam, M.M.A.; Evstishenkov, N.;Nawrot, N.; Villa, A.; Wojciechowska,E.; Kuittinen, S.; Pappinen, A. BiomassProduction and Removal of Nitrogenand Phosphorus from ProcessedMunicipal Wastewater by Salixschwerinii: A Field Trial. Water 2021,13, 2298. https://doi.org/10.3390/School of Forest Sciences, University of Eastern Finland, Yliopistokatu 7, P.O. Box 111, 80100 Joensuu, Finland;[email protected] (E.K.); [email protected] (M.M.A.S.); [email protected] (N.E.);[email protected] (A.V.); [email protected] (S.K.)Natural Resources Institute Finland (LUKE), Yliopistokatu 6, 80100 Joensuu, FinlandFaculty of Civil and Environmental Engineering, Gdansk University of Technology, 80-233 Gdansk, Poland;[email protected] (N.N.); [email protected] (E.W.)Correspondence: [email protected] (M.M.); [email protected] (A.P.)Abstract: In many Baltic regions, short-rotation willow (Salix spp.) is used as a vegetation filter forwastewater treatment and recycling of valuable nutrients to upsurge bioeconomy development. Inthis context, a four-year field trial (2016–2019) was carried out near a wastewater treatment plant ineastern Finland (Outokumpu) to investigate the effect of the processed wastewater (WW) on biomassproduction as well as the nutrients uptake capability (mainly N and P) by a willow variety (Salixschwerinii). Results indicated that WW irrigation expressively increased the willow diameter growthand biomass yield around 256% and 6510%, respectively, compared to the control treatment site(without WW). The willow was also able to accumulate approximately 41–60% of the N and 32–50%of the P in two years (2018–2019). Overall, willow showed a total 20% mortality rate under WWirrigation throughout the growing periods (2017–2019) as compared to control (39%). The resultsdemonstrate that willow has the potential to control eutrophication (reducing nutrients load) fromthe wastewater with the best survival rate and can provide high biomass production for bioenergygenerations in cold climatic conditions.w13162298Keywords: water pollution; wastewater reuse; nutrient; nature-based solution; willowAcademic Editor: William FrederickRitterReceived: 13 July 2021Accepted: 20 August 2021Published: 22 August 2021Publisher’s Note: MDPI stays neutralwith regard to jurisdictional claims inpublished maps and institutional affiliations.Copyright: 2021 by the authors.Licensee MDPI, Basel, Switzerland.This article is an open access articledistributed under the terms andconditions of the Creative CommonsAttribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).1. IntroductionNitrogen (N) and phosphorus (P) are essential nutrients for all living organisms, buthigher concentrations can exert a negative impact on the ecosystem. Technologies to recoveressential nutrients from the processed wastewater have become highly essential due to theincrease in fertilizers prices and strict discharge limits on excessive mineral nutrients [1].The overall sustainability of wastewater treatment plants can be upgraded by reducing theuse of non-renewable resources, minimizing waste generation, and implementing resourcerecycling approaches [2]. In many countries, municipal wastewater contains a sufficientamount of P and N and is recognized as a valuable resource. It could be favorable forboth agroforestry sectors and achieving food security once it has been properly treated.Therefore, wastewater can be a valuable source of organic fertilizer if effective recoveryprocesses are adopted [3].In Finland, all the municipal wastewater facilities are required to remove P and N asper the legal limits. According to Finnish Environmental Institute [4], the Finnish riverscarry an annual average of 74,000 tons of N and 3400 tons of P into the Baltic Sea, whichmainly comes from agricultural effluents and domestic wastewater. Long-term sustainability and nutrient self-sufficiency can be achieved if these nutrients in the wastewater arerecycled using a nature-based and cost-friendly method such as phytoremediation [5].Water 2021, 13, 2298. com/journal/water

Water 2021, 13, 22982 of 15Phytoremediation is an eco-friendly and cost-effective method for remediating polluted soils and wastewater by fast-growing and high biomass producing plants to accumulate metals/nutrients from the soil and water into plant biomass [6]. It has been reportedthat the resulting biomass after remediation can be used for energy and heat generations inbiorefineries and could become an environmentally friendly form of biotechnology andpromote bioeconomy development [7]. Further, plant-associated microorganisms commonly named “phytomicrobiome”, for example, epiphytes, endophytes, root microbiome,and phyllosphere microbiota, as well as bacteria and fungi, can be used in agriculture,pharma, and medicinal industries for environmental protection. These microbiomes produce divergent bioactive molecules that support the metabolization of greenhouse gasesand metals and hydrocarbons degradation [8].Previously, recovery of up to 650 and 100 kg/ha of N and P, respectively, has beenreported for annual and woody species under processed municipal wastewater (WW)irrigations [9]. Salam et al. [10,11] have also reported a significant accumulation of Nand P by two willow cultivars, including Salix schwerinii and Klara (Salix viminalis x Salixschwerinii x Salix dasyclados) irrigated with WW under greenhouse conditions.Willows (Salix spp.) is considered an effective tool to eliminate the heavy metals/metalloids from polluted sites [12,13]. In cold climatic regions such as Finland, the use ofshort-rotation willow to treat WW presents a potential solution and an innovative way ofwastewater and polluted groundwater purification as well as nutrient recovery (N and P)that require low construction and operating costs. Willows have unique characteristics suchas fast growth in boreal climate, high biomass production, bioenergy potential, remarkablemetabolic and absorption capabilities, deep-rooted system, high evapotranspiration rate,and ability to uptake a variety of pollutants and nutrients into their biomass, which makethem suitable for numerous environmental applications [14,15].Furthermore, phytoremediation could also be used to remediate eutrophicated water(high level of N and P), which has recently become global water pollution, includingFinland, due to the rapid industrialization, urbanization, and excessive agricultural practices. Eutrophicated water has ecological consequences on aquatic ecosystem functions,processes, and structures such as fast growth of algae and other phytoplankton deterioratethe water quality and subsequently affect the sustainable use of water resources [16]. TheGulf of Finland (Baltic Sea) and many Finnish lakes are suffering from eutrophication,which is considered an emerging domestic problem. In addition, current Finland’s N and Plevels have been doubled from the previous levels. To tackle this problem, nutrient runoffmust be reduced more efficiently, particularly in the agriculture and industrial sectors [17].The use of WW in agriculture could provide an alternative source of freshwater usefor irrigation and could also be an additional source of nutrients and organic matter. It canalso modify the minerals, macro-and micronutrients for plant growth, soil pH, soil buffercapacity, and cation exchange capacity [18]. Globally, processed municipal or industrialwastewater is used for the irrigation of about 20 million ha of crops worldwide. In Mexico,around 70,000 ha of agricultural lands are irrigated with WW, and more than 75% of theWW is used for crop irrigation in the USA [19]. Furthermore, the reuse of wastewater forcrop irrigation could contribute to mitigating water shortage, support the agriculture sectorand protect groundwater resources [20], and can also enhance the economic benefits forfarmers due to the reduced need for fertilizer [21].To the best of our knowledge, many studies have been focused on untreated wastewater, but very little attention has been paid concerning the effects of WW irrigation onshort-rotation crops such as willow as the results would provide insight about re-use ofwastewater for crops irrigation to reduce pressure on freshwater usage and dependency onchemical fertilizers. We hypothesize that willow plantations would accumulate the highestamount of nutrients from the WW and produce high biomass yield under WW irrigation.Therefore, this study aims to examine the effects of WW on the growth diameter of willowand total dry biomass production as well as total N and P accumulation by willow onceexposed to WW irrigation.

Water 2021, 13, 2298the highest amount of nutrients from the WW and produce high biomass yield under WWirrigation. Therefore, this study aims to examine the effects of WW on the growth diameterof willow and total dry biomass production as well as total N and P accumulation bywillow once exposed to WW irrigation.3 of 152. Materials and Methods2.1. Study Site and Experimental Setup2. Materials and MethodsA field trial was established adjacent to a municipal wastewater treatment plant in2.1. Study Site and Experimental SetupJokipohja Outokumpu (62 42′44.6″ N 29 02′58.5″ E) Eastern Finland. The Jokipohja plantA field trial bywasinitialestablishedadjacentto a municipalwastewatertreatmentplantis characterizedmechanicaltreatmentof wastewaters,chemicalremovalofinP 420 44.600 N 29 020 58.500 E) Eastern Finland. The Jokipohja plantJokipohjaOutokumpu(62with ferrous sulfate (FeSO4), polymers and lime (CaO), and secondary treatment of actiischaracterizedby localinitialstainlessmechanicalof wastewaters,chemicalremovalP withvatedsludge. Thesteeltreatmentmetal industryand the Jyrilandfillarea ,andsecondarytreatmentofactivated4tokumpu also transfer their wastewaters to the plant for purification. The wastewatersludge.Thelocal stainlessmetalloadindustrythe Jyri landfillareainhabitants,of the Outokumpuplant hasa capacityfor ansteelorganicfrom andapproximately10,000and cation.Thewastewaterplant(BOD)has a3 1average flow was observed around 3750 m day . The biological oxygen 000inhabitants,andtheaverageflowand chemical oxygen demand(COD) values of untreated wastewater varied from 490to3 day 1 . The biological oxygen demand (BOD) and chemicalwas observedaround3750m630 mg L 1 and 1200 to 1500 mg L 1, respectively.oxygen demand (COD) values of untreated wastewater varied from 490 2to 630 mg L 1 andThe experimental plots in Outokumpu were set up in a 3000 m area close to the1200 to 1500 mg L 1 , respectively.Lahdenjoki river. Another experimental plot in Siikasalmi (62 30′43.8″N 29 21′44.2″ E)The experimental plots in Outokumpu were set up in a 3000 m2 area close to thewith an area of 3000 m2 was considered as a reference control. Bothexperimentalplots areLahdenjoki river. Another experimental plot in Siikasalmi (62 300 43.800 N 29 210 44.200 E)shown in Figure 1. uttingsofwith an area of 3000 m2 was considered as a reference control. Both experimental plots arewillow (length: 20 cm; diameter: 15 mm; weight: 10 g) were collected from the Siikasalmishown in Figure 1. The soil properties from both study areas were identical. Cuttings ofexperimental area of the University of Eastern Finland. Willow cuttings were plantedwillow (length: 20 cm; diameter: 15 mm; weight: 10 g) were collected from the Siikasalmimanually to the soil in June 2016 in pair rows where the row spacing was 1 m, and theexperimental area of the University of Eastern Finland. Willow cuttings were plantedspacing between the pair rows was 150 cm. Rows were covered with black plastic to premanually to the soil in June 2016 in pair rows where the row spacing was 1 m, and thevent weeds from growing. The planting density of the willow was around 24,000 per hecspacing between the pair rows was 150 cm. Rows were covered with black plastic to preventtare. from growing. The planting density of the willow was around 24,000 per hectare.weedsFigure 1.1. The location of wastewater treatment plant (WWTP)(WWTP) andand willow experiment plot (EP) in Jokipohja (CEP)inSiikasalmi.and control experimental plot (CEP) in Siikasalmi.2.2. Scheme of Processed Wastewater (WW) Irrigation and Weather ConditionsThe flow of processed wastewater (WW) from the wastewater plant was carried outby automatic systems. WW irrigation to the field was delivered by a specially adjustedpipe connected to the mainstream pipe (Figure 2). The water flow meter was installed tomonitor the water load to the experimental field. The pipes were installed after the surfacewas leveled out, and the WW from the wastewater plant was pumped to the experimental

2.2. Scheme of Processed Wastewater (WW) Irrigation and Weather ConditionsWater 2021, 13, 2298The flow of processed wastewater (WW) from the wastewater plant was carried outby automatic systems. WW irrigation to the field was delivered by a specially adjusted4 of 15pipe connected to the mainstream pipe (Figure 2). The water flow meter was installedtomonitor the water load to the experimental field. The pipes were installed after the surfacewas leveled out, and the WW from the wastewater plant was pumped to the experimentalfield,where thethe WWWW waswas thenthen distributeddistributed withwith thinnerthinner pipepipe o