Microwave pyrolyzed sewage sludge: influence on soil microbiology, nutrient status, and plant biomass

Lono ae al. Chem. Biol. Technol. Ag ic. (2022) 9:92 h ps://doi.o g/10.1186/s40538-022-00354-8 RESEARCH Mic owa e py olyzed sewage sludge: in luence onsoil mic obiology, nu ien s a us, andplan biomass Kamila Lono a1, Ji i Hola ko2,3, Te eza Hamme schmied 2, Ludmila M a co a4, Ji i Kuce ik4, Adnan Mus a a2,4,5*, An onin Kin l2,6, Muhammad Na eed7, Jakub Racek8, Ma ie G ulicho a1, Ma a Miklaso a4 and Ma in B nicky2,4* Abs ac Backg ound: Sewage sludge (SS) has been conside ed a po en sou ce o soil nu ien s. Howe e , i s di ec applica- ion o ag icul u al soils ha e been discou aged owing o i s oxic na u e. The e o e, con e sion and modi ica ion o SS o dec ease i s oxici y has esul ed in ad anced me hods. Co-py olysis o SS wi h o he amendmen s is an ideal ea men esul ing in an en i onmen ally sa e and nu ien ich inal p oduc s wi h addi ional p ope ies o seques e ca bon. In he p esen s udy, a no el biocha was p oduced h ough he mic owa e py olysis o SS mixed wi h zeoli e and sawdus . The py olysis p oduc was hus cha ac e ized o elemen al composi ion, polycyclic a oma ic hyd oca - bons, ia Fou ie T ans o m In a ed Spec oscopy (FTIR), and o i s e ec s on soil mic obial cha ac e is ics, soil heal h and plan biomass a e soil applica ion. Resul s: Resul s e ealed ha , he SS modi ica ion esul ed in s able p oduc wi h highe nu ien s which u he depend on he ype and a io o eeds ock used. I s applica ion o soil signi ican ly imp o ed soil chemical and mic o- biological p ope ies and al e ed le uce biomass. Conclusions: We concluded ha sawdus eeds ock p omo ed nu ien a ailabili y in he esul ing biocha and induced highe ac i i y o nu ien mine alizing enzymes, whe eas zeoli e slowed down he elease o nu ien s om soil and pu a i ely immobilized enzymes. This join e ec o sewage sludge biocha , sawdus and zeoli e bene i ed he plan acquisi ion o nu ien s in compa ison wi h he mic obial nu ien up ake. We hus conclude ha mic owa e py olyzed SS could be used as a soil enhance . Keywo ds: Sus ainable ag icul u e, Soil quali y, Bio s imulan s, Nu ien cycling, Py olysis © The Au ho (s) 2022. Open Access This a icle is licensed unde a C ea i e Commons A ibu ion 4.0 In e na ional License, which pe mi s use, sha ing, adap a ion, dis ibu ion and ep oduc ion in any medium o o ma , as long as you gi e app op ia e c edi o he o iginal au ho (s) and he sou ce, p o ide a link o he C ea i e Commons licence, and indica e i changes we e made. The images o o he hi d pa y ma e ial in his a icle a e included in he a icle’s C ea i e Commons licence, unless indica ed o he wise in a c edi line o he ma e ial. I ma e ial is no included in he a icle’s C ea i e Commons licence and you in ended use is no pe mi ed by s a u o y egula ion o exceeds he pe mi ed use, you will need o ob ain pe mission di ec ly om he copy igh holde . To iew a copy o his licence, isi h p:// c ea i eco mmons. o g/ licen ses/ by/4. 0/. The C ea i e Commons Public Domain Dedica ion wai e (h p:// c ea i eco mmons. o g/ publi cdoma in/ ze o/1. 0/) applies o he da a made a ailable in his a icle, unless o he wise s a ed in a c edi line o he da a. Open Access *Co espondence: adnanmus a [email protected]; Ma in.B [email protected] 2 Depa men o Ag ochemis y, Soil Science, Mic obiology and Plan Nu i ion, Facul y o Ag iSciences, Mendel Uni e si y in B no, 613 00 B no, Czech Republic Full lis o au ho in o ma ion is a ailable a he end o he a icle Page 2 o 20 Lono ae al. Chem. Biol. Technol. Ag ic. (2022) 9:92 In oduc ion Cu en ly, municipal was e managemen has eme ged as a se ious socie al issue. In his ega d, a challenging issue is he inc ease in he olume o sewage sludge was e (SS), he ea men o which needs ene gy-in ensi e and cos ly p ocesses and sa e disposal me hods [1]. The Com- mission by he membe s a es o he Eu ope epo ed ha mo e han 10 million ons o d y biosolids includ- ing sewage sludge (SS) a e being gene a ed in EU annu- ally [2]. This amoun is he esul o he implemen a ion o Eu opean Union Di ec i e, he U ban Was ewa e T ea men 91/271/EEC and in oduc ion o ad anced echnologies in de elopmen o was ewa e ea men plan s (WWTP). In Eu opean Union (EU), nea ly, 37% o he annually p oduced d y biosolids (~ 3.6 million ons) ha e been ecycled in ag icul u al ac i i ies [2] di ec ly h ough con en ional me hods used o sewage sludge (SS) disposal o incine a ed, compos e c. Cu en ly, ecycling o land (di ec ly o ia compos ed SS) has been conside ed among he mos bene icial and economi- cal way o municipal SS managemen [3]. Ne e heless, despi e o many posi i e impac s o ecycling, he e a e many isks o SS applica ion including he in oduc ion o eme ging con aminan s (mainly high concen a ion o hea y me als, o ganic oxic compounds, pa hogens and mic oplas ics) in soil which, may con amina e he ood chain o ha m he en i onmen by su ace uno in o ecei ing wa e s [4]. The e o e, he e is an inc easing in e es o de eloping al e na i e me hods o SS ea men , in pa icula he - mal p ocessing me hods such as monoincine a ion, co- incine a ion, gasi ica ion, hyd o he mal ca bona ion, and py olysis ha e gained momen um in he cu en e a [5– 7]. Py olysis in his sense is a p ocess o he mal anoxic con e sion o o ganic ma e ials p oducing gas, oil and solid py olyzed esidue. This echnology o SS p ocessing can be highly ad an ageous, since i educes up o 50% o he was e olume [8] and s abilizes he o ganic ma - e (OM) in SS. In addi ion, he liquid and gaseous p od- uc s can be used as a uel, whe eas he ca bon- ich, solid by-p oduc (cha ) ha e a ious ag icul u al and echno- logical applica ions [6]. In pa icula , i is called biocha when applied o soil [9], while when applied echnologi- cally, i is called cha coal o coke [10]. Using biocha as he soil amendmen o e ilize is he subjec o many ecen s udies. I is known ha bio- cha can modula e he plan up ake o di e en nu ien s o po en ially oxic chemical subs ances and elemen s, such as hea y me als. Reduc ion o hea y me als concen- a ions and hei leachabili y om ishpond sedimen en iched wi h biocha was es ablished by Mehmood e al. [11]. In he same s udy, i was obse ed ha biocha addi ion could also inc ease he concen a ion o plan s a ailable mac onu ien s, such as phospho ous, ni ogen o po assium. This bene icial e ec o biocha could lead o highe yield o plan biomass p oduc ion as well as he G aphical Abs ac Page 3 o 20 Lono ae al. Chem. Biol. Technol. Ag ic. (2022) 9:92 po en ial use o con amina ed soil o he c op p oduc- ion due o immobiliza ion o oxic elemen s, such as he cadmium [12]. The e iciency o his e ec is dependen on he p ope ies o biocha which a e de i ed om he sou ce o biocha , biocha pa icle su ace, pH and he way o biocha p oduc ion. Condi ions o py olysis, such as empe a u e, esidence ime, hea ing a e, eeds ock pa icle size de e mine bo h he physical and chemical pa ame e s o esul ing biocha [13–15]. The p ope ies o eeds ock in luence he ace elemen con en (con- aminan s o a oma ic subs ances) and also i s po en ial o be used in ag icul u e [16–18]. Depending on condi- ions o py olysis and ype o SS [15], biocha s ob ained om SS py olysis a e highly mac opo ous, wi h he small olumes o he meso- and mic o-po es [19] among o h- e s, e.g., wood-de i ed biocha . Howe e , one should bea in mind ha he py olysis condi ions egula e he a ailabili y and oxici y o eme ging con aminan s [20, 21]. Fo ins ance, i has been epo ed ha , py olysis a lowe empe a u e o 300°C esul ed in he signi i- can educ ion in DTPA (die hylene iaminepen aace ic acid)-ex ac able me als in he SS-de i ed biocha [14]. Ano he s udy showed ha SS con e sion o biocha signi ican ly educes he con en o PAHs (polya oma ic hyd oca bons) and hei oxici y [22]; howe e , py olysis inc eased ace me als con en in esul ing p oduc due o a dec ease in esul ing mass (Pb, Cd, Zn, Cu, Ni and C ) [20, 23]. O he s udies also epo ed educed concen- a ion o ola ile o ganic compounds a highe py oly- sis empe a u es (up o 600°C). In addi ion, inc eased empe a u e led o inc eased con en o s able a oma ic ca bon, ash, some mac o- (Ca, Mg, P, and K) and mic o- nu ien s (Cu and Zn) and inc eased alkali eac ion [20]. Ne e heless, a sui able empe a u e o he SS py olysis can be used o ans o m bioa ailable hea y me als in o less soluble o ms [21, 23]. Addi ion o zeoli e (o gano-mine al so ben ) o sewage sludge eeds ock be o e py olysis ep esen s e icien app oach o imp o ing he quali y o SS biocha . Simila en ichmen o (compos ed) SS wi h zeoli e b ough he highe wa e -soluble and o al mac o-nu ien con en , as well as lowe phy o oxici y o he ob ained blended o gano-mine al ma e [24]. Co-py olysis o p e-biocha eeds ock and ben oni e o kaolin inc eased chemical and he mal s abili y, ecalci- ancy, a oma ic s uc u es in biocha [25, 26], o he co- py olyzed o gano-mine al clays and biocha imp o ed so p ion abili y o p oduc s: he p oduced biocha s e icien ly bound cip o loxacin [27], emo ed C (VI) om aqueous solu ion [28], mi iga ed g eenhouse gas emissions (GHG) by so p ion o CH4 and N2O emi ed om soil [29]. Ano he app oach o dec ease he oxic- i y o SS-con amina ing hea y me als is co-py olysis o SS wi h o he biomass [30–35]. Co-py olysis o SS wi h wooden (bamboo sawdus , willow sawdus ) o o he lignocellulo ic ( ice s aw) o ganic ma e ials educed he mobili y and bioa ailabili y o hea y me als in he inal biocha s [31, 33, 34]. Howe e , concu en e ec o he addi ion o co-py olyzed biomass educed yield, he mal s abili y, su ace a ea, and po e olume o bio- cha s, al hough he con en s o o ganic ma e and ca - bon in biocha s signi ican ly inc eased [31, 33]. Jin e al. showed he inc eased numbe o P–H (phospho us– hyd ogen) bonds (in phosphine) unde co-py olyzed biocha s as e ealed by Fou ie -T ans o m In a ed Spec oscopy (FTIR) analysis [33]. The eeds ock con- sis ing o SS and pinewood sawdus (1:1 w/w) [30] o bagasse [35] educed apo iza ion o gaseous ca bona- ceous p oduc s (a oma ic compounds, ke ones, CO2), while ola iliza ion o ni ogen-con aining p oduc s (i.e., NH3) and sulphu compounds was minimized [35]. Cu en ly, he in e es in p oducing SS biocha has gained momen um. The esea ch is ocused on he wide ange o SS biocha applica ions. One o hese app oaches is he use as a soil amendmen . Thus, bio- cha p oduced om SS blended wi h o he ype o biomass may be imp o ed in i s nu ien con en and binding p ope ies. This biocha used as soil amend- men s, could ha e he bene icial e ec o educe leaching o soil nu ien s, o enhance he e ilizing p ope ies, and nu ien e en ion capaci y in deg aded soils [36–40]. Based on many o he s udies, i seems ha using o SS biocha in ag icul u e as he soil amendmen o e ilize is he po en ially bene icial s a egy. The e iew by Xiao e  al. (2022) [41] men- ioned posi i e e ec s o SS biocha : dec ease o des- o p ion capaci y in soil o PAHs, inc ease o he soil N e en ion, immobiliza ion o hea y me als—Cu [42], Pb and Cd [43, 44] e c. Taking his backg ound in o accoun , his wo k aimed o use he sawdus -blended SS o p oduce biocha wi h dec eased a ailabili y o oxic con aminan s and o u ilize he ca bon-en iched inal biocha o imp o emen o soil chemical and biologi- cal p ope ies, plan nu i ion and c op g ow h. I was in ended o compa e he e ec o co-py olyzed SS and zeoli e on he esul ing biocha p ope ies. Recen ly, nega i e o “no e ec ” o SS biocha on soil was also epo ed, e.g., no e ec on a ailable nu ien concen- a ion [45] o phy o oxic impac o ola ile o ganic compounds in SS (unless hey we e emo ed by sho washing o wea he ing) [46]. Hence, he need o u - he esea ch on biocha SS as a po en ial soil ac i a o and e alua ion o i s bene i s migh be highly desi e- able. The e o e, he speci ic objec i es o his wo k we e o (i) assess he e icacy o alue addi ion o zeoli e and sawdus in co-py olyzed SS in e ms o inc eased soil Page 4 o 20 Lono ae al. Chem. Biol. Technol. Ag ic. (2022) 9:92 nu ien con en s and educed PAHs and (ii) e alua e he e ec s o soil applied co-py olyzed SS on mic obial soil heal h indica o s and plan biomass. To achie e he objec i es, ollowing hypo heses we e es ed. Ma e ials andme hods Biocha p epa a ion andcha ac e iza ion T ea men s o biocha we e p epa ed by mic owa e py olysis om SS mixed wi h zeoli e o /and sawdus , as shown in Table1. Biocha was applied o soil in 3 doses co esponding o he indica ed weigh pe cen ages o biocha in soil: 2.5%, 5% and 7.5% (25, 50, 75 ⋅ha−1). The sludge was ob ained om he municipal WWTP. Sewage wa e andsludge cha ac e iza ion andp ocessing The WWTP has a capaci y o a ound 530,000 popu- la ion equi alen s. WW is p edominan ly municipal WW o igina ing om households. Only 12–15% a e indus ial in luen s, bu gene ally his WW mos ly has he cha ac e o ypical municipal WW. Despi e he ela i ely low indus ial WW a io, SS ends o con- ain ela i ely high concen a ions o hea y me als. The anae obically diges ed SS was d ied using a con ac blade paddle d ye a empe a u e below 100°C. Tes ed aw d ied samples o SS (Fig.1) had d y solids a ound 91% and ou pu ac ion om d ye was a powde -like ma e ial wi h pa icle ac ion 1–8mm. Random es s e ealed ha he hyg oscopic wa e con en was below 2.0%. Pelle ized eeds ock The mix u es o d ied aw SS wi h e y ine sawdus ( om so wood) and zeoli e we e pelle ized by indus ial pelle izing p ess (Fig.2). In his wo k, a syn he ic zeo- li e (Pu mol 13) was chosen—zeoli e- ype ZSM-5 wi h admix u es o o he zeoli es ( aujasi e, wassali e) wi h a ineness o abou < 100µm. This syn he ic zeoli e has demons a ed he e iciency o he p ocess o mic owa e depolyme iza ion o lignocellulosic biomass [47]. Fo hese expe imen s, he pelle iza ion p ocess used an ex usion die ha ing diame e o 6.4mm. The em- pe a u e du ing pelle iza ion was measu ed on he me al ma ix o he pelle ize . The py olyzed eeds ock we e app ox. 6.4mm diame e pelle s o mixed SS wi h addi- i es made by pelle izing p ess (Fig.3). Table 1 T ea men s amended wi h biocha p epa ed om sewage sludge, sawdus , and zeoli e T ea men Composi ion o biomass o py olysis Abb e . 2.5 w % biocha (sewage sludge + zeoli e) 95 w % SS + 5 w % zeoli e 2.5% BC (Z) 5 w % biocha (sewage sludge + zeoli e) 95 w % SS + 5 w % zeoli e 5% BC (Z) 7.5 w % biocha (sewage sludge + zeoli e) 95 w % SS + 5 w % zeoli e 7.5% BC (Z) 2.5 w % biocha (sewage sludge + sawdus ) 75 w % SS + 25 w % sawdus 2.5% BC (SD) 5 w % biocha (sewage sludge + sawdus ) 75 w % SS + 25 w % sawdus 5% BC (SD) 7.5 w % biocha (sewage sludge + sawdus ) 75 w % SS + 25 w % sawdus 7.5% BC (SD) 2.5 w % biocha (sewage sludge + sawdus + zeoli e) 75 w % SS + 20 w % sawdus + 5 w % zeoli e 2.5% BC (SD + Z) 5 w % biocha (sewage sludge + sawdus + zeoli e) 75 w % SS + 20 w % sawdus + 5 w % zeoli e 5% BC (SD + Z) 7.5 w % biocha (sewage sludge + sawdus + zeoli e) 75 w % SS + 20 w % sawdus + 5 w % zeoli e 7.5% BC (SD + Z) Fig. 1 Raw d ied sewage sludge Fig. 2 Pelle ized aw ma e ial Page 5 o 20 Lono ae al. Chem. Biol. Technol. Ag ic. (2022) 9:92 Mic owa e py olysis uni Expe imen s we e pe o med by slow mic owa e py oly- sis uni which wo ks a low p essu e 800hPa. Mic owa e was gene a ed by magne on wi h 3.0kW inpu powe , egula ed ou pu powe , and wi h 2.45GHz. This uni wo ks discon inuously, and he maximum capaci y is app ox. 3kg∙ba ch−1 o eeds ock. The glass condense a ached o he py olyze was used o he sepa a ion o gaseous p oduc s and he oil. Fo incoming and e lec ed wa es a une was ins alled. The in a ed (IR) he mome- e was in oduced in o he cen e o he inpu eeds ock. The inpu weigh o eeds ock samples was 1.0kg·ba ch−1. Du ing he expe imen s, he ou pu eg- ula ed powe o magne on was 1.2kW, esidence ime was 60min, and he empe a u e du ing he es s did no exceed 250°C. Fou ie ans o m in a ed spec oscopy (FTIR) analysis The Fou ie ans o m in a ed spec oscopy (FTIR) spec a o he ob ained biocha samples was eco ded on a B uke di used e lec ance in a ed Fou ie ans o m (DRIFT) spec ome e . The spec a we e collec ed a ansmission mode be ween 4000 and 400 cm−1 wi h es- olu ion o 8 cm−1 and 128 scans using OPUS compu e - based so wa e. P io analysis he samples we e p epa ed by mixing wi h KB o o m a homogenous mix u e. Polya oma ic hyd oca bons (PAH) de e mina ion in esul ing biocha The ex ac ion o homogenized samples (1g o g ounded BC sample, Re sch MM 200) was ca ied ou by p essu - ized sol en ex ac ion (one PSE, Applied Sepa a ions). Toluene was used as a sol en , he ex ac ion was ca ied ou a 130°C, 120ba and 3 cycles. Be o e ex ac ion, in e nal s anda d (100 /10 ul, 5 deu e a ed PAH) was added o samples. Toluene was e apo a ed o app oxi- ma ely 1 mL o inal olume. Gas ch oma og aphy wi h mass spec ome y (B uke EVOQ GC-TQ) was used o he analysis o 16 EPA PAHs in he ex ac s. 16 EPA PAHs we e sepa a ed in column DB-EUPAH (20m × 0.180mm; 0.14 um), he empe a u e p og am was 80°C o 1min, hen an inc ease o 320°C (5min) wi h hea ing a e 15°C/min, spi less injec ion a 270°C, EI 70eV, SIM mode. Quan i ica ion was ca ied ou by in e nal s anda d calib a ion. PO4 de e mina ion Fo he analysis o PO4–P in wa e leacha e (5g o BC and 50ml o MilliQ wa e , il a ion a e 24h) was used he spec opho ome ic me hod acco ding ČSN EN ISO 6878 (MQuan TM Phospha e Tes , Me ck) [48]. De e mina ion o leachable hea y me als Hea y me als such as me cu y (Hg), cuppe (Cu), ch o- mium (C ), zinc (Zn), led (Pb), a senic (As), nickel (Ni) and cadmium (Cd) we e de e mined in he wa e ex ac using a omic abso p ion spec ome e wi h elec o he - mal a omiza ion ZEEni 60 om Analy ik Jena (Ge - many) wi h Zeeman backg ound co ec ion and selec ed hollow ca hode lamp by Pho on (Aus alia) acco ding o he me hod desc ibed in he wo k o Racek e al. (2019) [49]. Po expe imen s andsampling The po expe imen wi h le uce (Lac uca sa i a L. a . B ilan ; SEMO a.s, Czech Republic) was pe o med in 1-L capaci y po s. The po s we e illed up wi h 300g o comme cial ga den subs a e TS 3 medium basic 425 s anda d (Klasmann–Deilmann GmbH, Ge many), ho - oughly mixed wi h a dose o biocha acco ding o ea - men s epo ed in Table1. The subs a e was a mix u e o ligh pea (0–25mm) wi h we ing agen , d y ma e 45%, pH 6.0, sal s 1g L−1, nu ien con en (acco ding o man- u ac u e ): N 140mg⋅L−1, P 44mg⋅L−1, K 150mg⋅L−1, Mg 100mg⋅L−1. Al oge he , 10 ea men s we e es ed (subs a e amended wi h 9 ypes/doses o biocha , and unamended subs a e = nega i e con ol), each ea men was p epa ed in ou eplica es. Th ee seeds we e sown in each po , hen wa e ed wi h 200mL o deionized wa e . A e a week o ge mina ion, only one plan pe po was es ablished. The wa e ing was egula ly ca ied ou du ing cul i a ion o main ain he same soil mois u e and plan s did no wil . The expe i- men was ca ied ou o 8weeks in g eenhouse unde con olled condi ions (day/nigh ): empe a u e 22/18°C, ela i e ai humidi y 50/50%, pho ope iod 14/10h. A he end o he cul i a ion, he chlo ophyll a luo escence in da k adap ed lea es was measu ed and he abo e g ound plan biomass was ha es ed o he analyses o pigmen s, Fig. 3 Biocha Page 6 o 20 Lono ae al. Chem. Biol. Technol. Ag ic. (2022) 9:92 and o plan esh and d y biomass es ima ion. In addi- ion, mixed soil sample was aken om each po o de e mina ion o basic physical, chemical and biological soil quali y indica o . Plan biomass quan i ica ion andquali y pa ame e s de e mina ion Le uce esh abo eg ound biomass (AGB) was de e - mined g a ime ically by weighing he shoo s on he labo a o y scales. To de e mine plan d y biomass, esh plan ma e ial was d ied a 60°C o cons an weigh and ob ained d y biomass was again es ima ed g a ime i- cally. D y ma e con en in esh plan biomass was calcula ed (da a a e no p esen ed). Changes in he pho- osyn he ic appa a us we e e alua ed using chlo ophyll luo escence pa ame e s measu ed in da k adap ed lea es o in ac plan s using he po able luo ome e Fluo Pen FP 100 (Pho on Sys em Ins umen , Czech Republic). I was measu ed he as luo escen kine ic p esen ed as he OJIP ansien cu es. P io o d ying o esh plan biomass, 0.5 g o esh ma e ial was aken om each plan o de e mine he con en o lea pigmen s, lyophi- lized and s o ed a −18 °C. Lyophilized samples we e homogenized wi h 10mL ace one. Ace one ex ac s we e analyzed wi h spec opho ome e (Spe onic 20 Genesys, The mo Spec onic, USA) a wa eleng h 662, 645 and 470nm. The con en o indi idual pigmen s was calcu- la ed acco ding o he me hodology Lich en hale and Buschmann (2005) [50]. De e mina ion o soil quali y p ope ies The subs a e om each po was homogenized by sie ing i h ough 2mm mesh and s o ed a 4°C ( o de e mina- ion o soil espi a ion), lyophilized and s o ed a −18°C ( o de e mina ion o soil enzyme ac i i ies), and he es we e ai -d ied o quan i ica ion o nu ien con en and pH measu emen . Soil eac ion, pH (CaCl2)—was de e - mined acco ding o ISO 10390:2005 [51], dehyd ogenase (DHA) ac i i y was measu ed acco ding o Vobe ko a e  al. [52] and exp essed in µg ( iphenyl o mazan) TPF·g−1·h−1, o he enzyma ic ac i i ies—β-glucosidase (GLU), a ylsul a ase (ARS), phospha ase (Phos), u e- ase (U e) and N-ace yl-β-D-glucosaminidase (NAG)— we e measu ed spec opho ome ically acco ding o ISO 20130:2018 [53] and he alues exp essed in µmol (p-ni ophenol) PNP·g−1·h−1 and in µmol NH3·g−1·h−1 (u ease). S a is ical analyses Da a ob ained om he de e mina ion o plan biomass, quali a i e p ope ies, and soil chemical and biological pa ame e s we e s a is ically analyzed using he me hods o p incipal componen analysis (PCA), one-way analysis o a iance (ANOVA), Tukey HSD pos -hoc es (a sig- ni icance le el p = 0.05), and Pea son co ela ion analy- sis ia P og am R, e sion 3.6.1 [54, 55]. Fo es ing o he no mali y o dis ibu ion, i was used Kolmogo o and Smi no es and da a homoscedas ici y was exam- ined by Ba le ’s es , bo h a signi icance le els o 0.05. Besides, assump ions o all es s we e also checked by di e en diagnos ic plo s. The minimal le el o s a is ical signi icance o mos o he used me hods was 0.05. The esul s o Pea son’s co ela ion analysis we e in e p e ed (acco ding o he alue o co ela ion coe icien ) as ol- lows: 0.5 < < 0.7 (mode a e co ela ion) and 0.7 < < 0.9 (high co ela ion) [56]. Resul s Biocha cha ac e is ics and esul s o FTIR analysis The concen a ions o Hg, C , Pb, As and Cd in he wa e ex ac om biocha ypes we e below de ec ion lim- i s, o Cu i was 1mg L−1, o Zn 2.2mg L−1 and o Ni 0.7mg L−1. As he concen a ions o all he me als we e e y low and did no each minimal inhibi ion/ oxic le - els o plan s, hey a e no u he discussed in he ex . The o al ni ogen (N o ) and o al hyd ogen (H o ) con- en s we e bo h signi ican ly highes in he BC (SD) bio- cha and lowes in he BC (SD + Z) ea men (Fig.4). The mu ual a ios be ween mac oelemen s in he h ee biocha ypes showed signi ican di e ences oo. C:N a io was highes in he BC (SD + Z) biocha (a ound 12.0) and he lowes in he BC (Z) biocha (8.0). H:C a io on he o he hand was highes (> 1.0) in he BC (SD) bio- cha and he lowes (< 0.8) in he ea men BC (SD + Z). Simila ly, O:C was highes (> 0.4) unde biocha BC (Z), ollowed by BC (SD + Z) and BC (SD). These di e se esul s an icipa ed no signi ican mu ual co ela ions be ween he a io p ope ies (Fig.5). The signi ican ly highes con en o leachable phospha e (calcula ed o d y biocha weigh —a ound 600mg⋅kg−1) was de ec ed in he wa e leacha e o BC (SD) biocha , compa ed o he SD (Z) ea men (a ound 300mg⋅kg−1) and he lowes con en was in he BC (SD + Z) biocha (< 100 mg⋅kg−1). No signi ican di e ence in he sum con en o 16 EPA PAHs be ween all h ee biocha ypes was de ec ed. No co ela ion be ween PAH con en was obse ed wi h o he biocha p ope ies. The FTIR analysis o he h ee ypes o biocha sam- ples e ealed simila i ies in hei composi ion in e ms o a oma ic and alipha ic moie ies. Impo an ly, he biocha p epa ed om 25 w % sawdus (Fig.5B), which showed an enhanced in ensi y signal a 2927 cm−1, depic ing cha ac e is ic alipha ic C–H s e ching as compa ed o o he biocha ypes (Fig.5A, C). Mo eo e , unlike (25% sawdus ) and (5% zeoli e) de i ed biocha (Fig.5B, A), he (20% sawdus + 5% zeoli e) de i ed biocha (Fig.5C) lack Page 7 o 20 Lono ae al. Chem. Biol. Technol. Ag ic. (2022) 9:92 a cha ac e is ic peak be ween 3900 and 3500 cm−1, ep- esen ing OH-s e ching o ca boxyl unc ional g oups. Fu he mo e, all he h ee ypes o biocha showed s ong peak abo e 1500–400 cm−1, depic ing com- pounds de i ed om polysaccha ides (1057 cm−1), a o- ma ic C–H s e ches (1506 cm−1) and alipha ic amides (1557 cm−1) (Fig.5A, B, C). In addi ion, he C–H s e ch- ing ib a ions we e obse ed a 2970 and 2860 cm−1. This shows ha he co-py olysis o SS biocha wi h di e en a es o sawdus and zeoli e esul ed in al e ed unc ional g oup chemis y o esul an biocha samples. Soil eac ion andenzyme ac i i ies Soil eac ion pH (CaCl2) alue was signi ican ly lowes in he ea men s 2.5% BC (SD), 7.5% BC (SD), and 7.5% BC (SD + Z) as compa ed o con ol (Fig.6). The soil pH did no show any signi ican and conside able co ela ion wi h o he measu ed pa ame e s. The dehyd ogenase ac i i y (DHA) was inc eased in all ea men s excep o 2.5% BC (SD + Z) and 7.5% BC (SD + Z) as compa ed o he con ol (Fig.6). The highes DHA alue was de ec ed in he 2.5% BC (SD) ea men s and was inc eased as compa ed o all ea men s o con- ol, wi h BC (Z), wi h BC (SD + Z), and 7.5% BC (SD) ea men . The Pea son’s co ela ion analysis e ealed no Fig. 4 Chemical p ope ies o biocha ea men s made o sewage sludge, sawdus , and zeoli e, con en o A ni ogen, B oxygen, C ca bon, D hyd ogen, E ca bon and ni ogen a io, F hyd ogen and ca bon a io, G oxygen and ca bon a io, H concen a ion o phospho ous in o m o phospha e in wa e leacha e o biocha (mg·l−1), I concen a ion o phospha e in biocha (mg·kg−1), J concen a ion o 16 p io i y PAHs acco ding o U.S. EPA (mg·kg−1). Mean ± s anda d de ia ion (e o ba s) calcula ed om independen alues (n = 4), di e en le e s exp ess he s a is ical di e ences a signi icance le el p ≤ 0.05 Fig. 5 FTIR spec a o A 5% zeoli e–biocha , B 25% sawdus –biocha and C 20% sawdus + 5% zeoli e–biocha Page 8 o 20 Lono ae al. Chem. Biol. Technol. Ag ic. (2022) 9:92 signi ican and conside able co ela ion o DHA wi h any o he plan o soil p ope y. The ac i i y o a ylsul a ase (ARS) was inc eased in all ea men s wi h BC (SD), unde bo h 2.5% and 7.5% BC (Z), and 7.5% BC (SD + Z) as compa ed o con ol (Fig.7). The highes ARS alue was e ealed in he 7.5% BC (SD) as compa ed o all o he ea men s, while he low- es ARS was in 2.5% BC (SD + Z) and 5% BC (SD + Z) ela i e o all o he biocha -amended ea men s. The Pea son’s co ela ion analysis showed ha ARS was Fig. 6 Soil pH and dehyd ogenase ac i i y (DHA) o subs a e ea men s amended wi h biocha made o sewage sludge, sawdus , and zeoli e. Mean ± s anda d de ia ion (e o ba s) calcula ed om independen alues (n = 4), di e en le e s exp ess he s a is ical di e ences a signi icance le el p ≤ 0.05. Fig. 7 Soil enzyme ac i i ies—A a ylsul a ase (ARS), B u ease (URE), C phospha ase (PHOS), D N-ace yl-β-D-glucosaminidase (NAG), E β-glucosidase (GLU)—o subs a e ea men s amended wi h biocha made o sewage sludge, sawdus , and zeoli e. Mean ± s anda d de ia ion (e o ba s) calcula ed om independen alues (n = 36), di e en le e s exp ess he s a is ical di e ences a signi icance le el p ≤ 0.05 Page 9 o 20 Lono ae al. Chem. Biol. Technol. Ag ic. (2022) 9:92 signi ican ly (p ≤ 0.001) and mode a ely posi i ely co - ela ed wi h PHOS ( = 0.65), URE ( = 0.58), and GLU ( = 0.58) (Fig.8). The URE ac i i y was signi ican ly inc eased in ea - men s 2.5% and 7.5% BC (Z), 5% and 7.5% BC (SD), as well as 5% and 7.5% BC (SD + Z) as compa ed o he con ol. Howe e , he highes u ease ac i i y was de ec ed in he 7.5% BC (SD) ea men and he lowes was in 5% BC (Z), as compa ed o all o he ea men s. The URE showed mode a e posi i e and signi ican (p ≤ 0.001) co ela ion o PHOS ( = 0.61) and GLU ( = 0.66), espec i ely (Fig.8). PHOS was signi ican ly inc eased (compa ed o he con ol) in all h ee ea men s amended wi h BC (SD) a 2.5%, 5%, and 7.5% BC (SD). Mo eo e , 5% and 7.5% BC (SD) ea men s showed highe PHOS compa ed o any o he biocha amended ea men . The highes PHOS ac i i y was eco ded in 7.5% BC (SD) and he lowes was in 2.5% BC (SD + Z) as compa ed o con- ol and o he ea men s (Fig.6). We also obse ed a signi ican (p ≤ 0.001) co ela ion be ween PHOS and NAG (mode a e posi i e, = 0.51) and GLU (high posi- i e, = 0.79). N-ace yl-β-D-glucosaminidase (NAG) was inc eased in he ea men s 5% BC (SD), 7.5% BC (SD), and 2.5% BC (SD + Z) in compa ison wi h he con ol (Fig.7) and signi ican ly dec eased in 7.5% BC (SD + Z) in compa i- son wi h all o he ea men s. NAG co ela ed signi i- can ly (p ≤ 0.001) and mode a ely posi i ely wi h GLU ( = 0.6). The ac i i y o GLU was signi ican ly inc eased in all 3 ea men s wi h BC (SD) and BC (SD + Z) as well as in bo h 5% and 7.5% BC (Z), as compa ed o he con ol (Fig.7). The highes GLU alues we e obse ed o 5% BC (SD) and 7.5% BC (SD) as compa ed o con- ols and o he ea men s. Plan biomass andpho osyn he ic pigmen s The esh and d y abo eg ound (AGB) biomass showed no signi ican di e ence be ween all amended expe i- men al ea men s and he con ol as well (Fig.9). The con en o chlo ophyll a and b showed highly posi i e and signi ican co ela ion (p ≤ 0.001, = 0.96) in ou s udy. Thei alues we e conside ably dec eased in all h ee ea men s wi h BC (Z) and in 7.5% BC (SD + Z) ea - men , and signi ican ly inc eased only in 5% BC (SD + Z) ea men , as compa ed o he con ol (Fig.9). A signi ican dec ease in he chlo ophyll a/b a io was de ec ed in bo h 2.5% and 7.5% BC (Z) compa ed o he con ol. The o al ca o enoids con en was dec eased (as com- pa ed o he con ol) in all ea men s amended wi h BC (Z) addi i e. The highes alue was obse ed o 5% BC Fig. 8 Resul s o Pea son’s co ela ion analysis among soil and plan p ope ies. Values in he cells = co ela ion coe icien , calcula ed on he le el o signi icance p: ≤ 0.1 (⋅), ≤ 0.05 (*), ≤ 0.01 (**), ≤ 0.001 (***) Page 16 o 20 Lono ae al. Chem. Biol. Technol. Ag ic. (2022) 9:92 he p edic ion ha he long- e m cul i a ion o plan s could lead o obse a ion o posi i e e ec o he bio- cha addi ion due o he suppo o soil mic o lo a and imp o emen o nu ien a ailabili y especially in nu i- en poo soil [101]. Mic owa e py olyzed biocha —an amendmen o  e ilize ? Applica ion o biocha o soil ep esen s a s a egy o seques a ion o ca bon, because biocha ’s chemical s uc u e is conside ed o be esis an o mic obiological a ack [102]. Simul aneously, depending on he eeds ock and condi ions o p epa a ion, biocha may ep esen a sou ce o mac onu ien s and an amendmen imp o - ing wa e -holding capaci y. The Eu opean Biocha Ce - i ica e s a es ha , “Biocha is a cha coal-like subs ance ha is py olysed om sus ainable ob ained biomass unde con olled condi ions and which is used o any pu pose which does no in ol e i s apid mine aliza ion o CO2” [67]. Based on his de ini ion, Con e e al. [103] concluded ha biocha may be p oduced only om as g owing plan s, plan esidues om ce i ied o es y managemen , ag icul u al esidues, and o ganic was es om u ban a eas [103]. Howe e , py olysis o sewage sludge py olyzed unde condi ions (i.e., low empe a- u e mic owa e py olysis) used in his wo k appea ed o p oduce biocha ha is appa en ly biodeg adable and in ensi ely s imula es he ac i i y o soil mic oo gan- isms. We a ibu e his obse a ion o he in e play o wo impo an ac o s: empe a u e o he py olysis and used eeds ock. Acco ding o Tag e al., [104] he inc eas- ing empe a u e dec eases bo h he H:C and O:C a ios in py olyzed biomass, such as ine p uning (VP), poul y li e (PL), o ange pomace (OP) and seaweed [104]. Com- pa ing esul s wi h hose epo ed by Tag e al., (2016) oughly co espond o he dependence o O:C a espec- i e py olysis empe a u e, bu H:C a io is in ou case signi ican ly lowe [104]. In o he wo ds, biocha om sewage sludge is less a oma ic (see Fig.5) compa ing o o he sou ces, which con i ms he compa ison wi h o he au ho s [104–106]. In ac , eeds ocks o py olysis a e usually based on lig- nocellulose ma e ials, such as wood esidues, g ass and o he s. On he con a y, sewage sludge is o mic obio- logical o igin, i.e., i con ains mainly N- ich compounds om p o oplasma and cell memb anes, such as p o eins and a y acids. The e o e, esul ing s uc u e di e s com- pa ed o lignocellulose-based biocha ; he O:C is simila , bu lowe H:C in SS-based biocha shows ha his bio- cha is signi ican ly less a oma ic, i.e., mo e alipha ic. As i is well-known ha alipha ic s uc u es a e be e biode- g adable compa ing o a oma ic s uc u es [107], biocha p epa ed om sewage sludge ac s as mo e as a e ilize ins ead o an amendmen . This is suppo ed by highe con en o ni ogen in i s s uc u e, which seems o be also bioa ailable as sugges ed by ac i i y o u ease. Mic owa e py olysis is as , selec i e and e icien me hod o p oduc ion o py olyzed ma e ials [49, 108]. Howe e , he condi ions such a low empe a u e may lead o p oduc s whose p ope ies a e a om de ini ion o biocha . As ollows om he esul s, no e e y in en- ionally py olyzed o ganic ma e ial is sui able o ca bon seques a ion; ne e heless, i s e ec on soil may s ill be posi i e. In pa icula , i may ep esen a sou ce o labile ca bon ha suppo s soil mic obial p ocesses oge he wi h mac onu ien s. In addi ion, hese e ec s may be uned by addi ion o zeoli e, which ei he s abilizes he biocha s uc u e o mode a e elease o nu ien s. I emains a ques ion, i he py olyzed p oduc o sewage sludge should s ill be named as a biocha , as he biocha pe de ini ion, is mic obiologically s able ma e ial [67]. Mo eo e , i s applica ion is one o he keys in he long- e m s a egy o inc easing o soil o ganic ca bon in soils and seques a ion/s o age o ca bon in soil. Despi e he enhanced mic obial ac i i y o soil mic o- o ganisms, he use o his pa icula biocha nei he inc eased no dec eased biomass yield which can be explained as ollows: i) he amoun o N eleased om SS biocha was high enough o suppo he soil mic o- o ganism and no compe i ion be ween soil mic obiome and plan oo s o Lac uca sa i a occu ed and ii) he leng h o he expe imen was oo sho and he e ec on plan could no mani es , i.e., biocha a ec ed soil mic o- biological p ocesses, bu he e ec on plan s appea s wi h a delay, iii) hea y me als, he highe con en o which is usually a p oblem o he municipal SS [49], a ec ed nei- he soil mic obiome no plan which con i ms i s ixa- ion and immobiliza ion in biocha s uc u e [49]. Conclusions This s udy concluded ha mic owa e py olysis p o- duced biocha om sewage sludge exe ed a dec eased mic obiological s abili y o ca bonaceous con en and was pu a i ely less e icien in soil ca bon seques a- ion. The p oduced biocha signi ican ly a ec ed soil chemical and mic obiological p ope ies. In pa icula , soil pH was signi ican ly dec eased due o applica ion o biocha p oduced om sewage sludge and sawdus , whe eas dehyd ogenase, β-glucosidase, a ylsul a ase, phospha ase, u ease, N-ace yl-β-D-glucosaminidase was inc eased. Biocha applica ion le el was he c ucial ac- o in go e ning enzyme ac i i ies. Sawdus biomass p o- mo ed nu ien a ailabili y in he esul ing biocha s and induced highe ac i i y o nu ien mine alizing enzymes, whe eas zeoli e slowed down he elease o nu ien s om soil and pu a i ely immobilized enzymes. This join Page 17 o 20 Lono ae al. Chem. Biol. Technol. Ag ic. (2022) 9:92 e ec o sewage sludge biocha , sawdus and zeoli e ben- e i ed he plan acquisi ion o nu ien s in compa ison wi h he mic obial nu ien up ake. Howe e , his e ec was no accompanied wi h a changed le uce biomass yield as he esh and d y abo eg ound (AGB) biomass showed no signi ican di e ence be ween all expe imen- al ea men s. Albei he biocha SS + SD + Z (a dose 5% o sewage sludge) de e mined no imp o emen in quan- i y o le uce biomass, i showed he highes con en o pho osyn hesis pigmen (chlo ophyl a, b, ca o enoids) and ep esen an e en ual app oach in he p oduc ion o sewage sludge-based biocha wi h desi ed ai s o soil/ ag icul u al applica ion. Acknowledgemen s No applicable. Au ho con ibu ions AM, JH and MB: concep ualiza ion. KL, JR: me hodology. TH, KL, and LM: so - wa e. MN, JK, and AK: alida ion. MB, MM, LM and TH: o mal analysis. JR, MM and MG: esou ces. KL, MG, MM and AK: da a cu a ion. KL, JH: w i ing—o iginal d a p epa a ion. JK, AM, TH, MN, JR and MB: w i ing— e iew and edi ing. MB and JK: supe ision. KL, LM and JR: p ojec adminis a ion. KL, AK, JK and MB: unding acquisi ion. All au ho s ead and app o ed he inal manusc ip . Funding The wo k was suppo ed by he p ojec s o Technology Agency o he Czech Republic TJ02000261 and TH03030319, by he Minis y o Ag icul u e o he Czech Republic, ins i u ional suppo MZE-RO1218, MZE-RO1722 and by Minis y o Educa ion, You h and Spo s o he Czech Republic, g an numbe FCH-S-22-8001. A ailabili y o da a and ma e ials The da a se s used and/o analysed du ing he cu en s udy a e a ailable om he co esponding au ho on easonable eques . Decla a ions E hics app o al and consen o pa icipa e No applicable. Consen o publica ion No applicable. Compe ing in e es s The au ho s decla e ha hey ha e no compe ing in e es s. Au ho de ails 1 Depa men o Plan Biology, Facul y o Ag iSciences, Mendel Uni e si y in B no, B no 61300, Czech Republic. 2 Depa men o Ag ochemis y, Soil Science, Mic obiology and Plan Nu i ion, Facul y o Ag iSciences, Mendel Uni e si y in B no, 613 00 B no, Czech Republic. 3 Ag o yzkum Rapo in, L d., Vyzkumniku 267, 788 13 Rapo in, Czech Republic. 4 Ins i u e o Chemis y and Technology o En i onmen al P o ec ion, Facul y o Chemis y, B no Uni- e si y o Technology, Pu kyno a 118, 612 00 B no, Czech Republic. 5 I ns i u e o En i onmen al S udies, Facul y o Science, Cha les Uni e si y, Bena ska 2, 12800 P ague, Czech Republic. 6 Ag icul u al Resea ch, L d., 664 41 T oubsko, Czech Republic. 7 Ins i u e o Soil and En i onmen al Science, Uni e si y o Ag icul u e Faisalabad, Faisalabad, Pakis an. 8 AdMaS Resea ch Cen e, Fac- ul y o Ci il Enginee ing, B no Uni e si y o Technology, Pu kyno a 651/139, 61200 B no, Czech Republic. Recei ed: 9 Augus 2022 Accep ed: 31 Oc obe 2022 Re e ences 1. 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