Increasing Phylogenetic Clustering of Arbuscular Mycorrhizal Fungal Communities in Roots Explains Enhanced Plant Growth and Phosphorus Uptake

This is a sel -a chi ed e sion o an o iginal a icle. This e sion may di e om he o iginal in pagina ion and ypog aphic de ails. Au ho (s): Ti le: Yea : Ve sion: Copy igh : Righ s: Righ s u l: Please ci e he o iginal e sion: CC BY 4.0 h ps://c ea i ecommons.o g/licenses/by/4.0/ Inc easing Phylogene ic Clus e ing o A buscula Myco hizal Fungal Communi ies in Roo s Explains Enhanced Plan G ow h and Phospho us Up ake © The Au ho (s) 2024 Published e sion F ew, Adam; Aguila -T igue os, Ca los A. F ew, A., & Aguila -T igue os, C. A. (2024). Inc easing Phylogene ic Clus e ing o A buscula Myco hizal Fungal Communi ies in Roo s Explains Enhanced Plan G ow h and Phospho us Up ake. Mic obial Ecology, 87(1), A icle 139. h ps://doi.o g/10.1007/s00248-024-02457-1 2024 Vol.:(0123456789) Mic obial Ecology (2024) 87:139 h ps://doi.o g/10.1007/s00248-024-02457-1 BRIEF REPORT Inc easing Phylogene ic Clus e ing o A buscula Myco hizal Fungal Communi ies inRoo s Explains Enhanced Plan G ow h andPhospho us Up ake AdamF ew1,2,3 · Ca losA.Aguila ‑T igue os3 Recei ed: 9 Sep embe 2024 / Accep ed: 1 No embe 2024 © The Au ho (s) 2024 Abs ac Tempo al a ia ion du ing he assembly o a buscula myco hizal (AM) ungal communi ies wi hin plan oo s ha e been posi ed as c i ical d i e s o he plan - ungal symbio ic ou comes. Howe e , unc ional implica ions o hese dynamics o he hos plan emain poo ly unde s ood. We conduc ed a con olled po expe imen wi h So ghum bicolo o in es iga e how em- po al shi s in AM ungal communi y composi ion and phylogene ic di e si y in luence plan g ow h and phospho us esponses o he symbiosis. We cha ac e ised he oo -colonising AM ungal communi ies ac oss h ee ime poin s and explo ed hei communi y assembly p ocesses by analysing hei phylogene ic di e si y and employing join species dis ibu ion modelling wi h he Hie a chical Modelling o Species Communi ies (HMSC) amewo k. We ound s ong AM ungal u no e h ough ime wi h a high phylogene ic signal, indica ing ec ui men o phylogene ically clus e ed AM ungal species in he hos . This empo al phylogene ic clus e ing o communi ies coincided wi h ma ked inc eases in plan biomass and phospho us esponses o he AM ungal symbiosis, sugges ing ha hos selec ion o speci ic ungi may be a key de e minan o hese bene i s. Keywo ds A buscula myco hiza· Communi y assembly· Phylogene ic di e si y· So ghum bicolo Mos e es ial plan s engage in symbio ic associa ions wi h a buscula myco hizal (AM) ungi [1]. In his symbiosis, he ungi colonise plan oo s and he su ounding soil, acili a ing he plan ’s access o essen ial nu ien s such as phospho us, while acqui ing ca bon om he plan [2]. The composi ion o AM ungal communi ies exe s a conside - able in luence on he symbio ic e ec s expe ienced by he plan hos s [3–5]. Consequen ly, unde s anding he de e mi- nan s o AM ungal communi y composi ion has long been a ocus o ecological esea ch [6–8]. Howe e , achie ing his is complica ed by he global dis ibu ion o AM ungi, whose axa a e ound ac oss mul iple hos s and a wide a ay o en i onmen al condi ions [9]. Despi e hei widesp ead dis ibu ion, e idence sug- ges s ha en i onmen al il e ing plays a c i ical ole in he assembly o AM ungal communi ies [9]. Local-scale s udies o en e eal ha hese assemblages a e composed o closely ela ed indi iduals, sugges ing ha phylogene ic clus e ing occu s as communi ies change o sui speci ic habi a s [10]. In he con ex o oo -colonising communi ies, he oo sys- em o he hos plan se es as he local habi a o he ungi. These oo -colonising communi ies a e equen ly obse ed o be phylogene ically clus e ed [7], likely as a esul o bo h abio ic il e ing and mu ualis ic pa ne selec ion [11–13]. Wi h e idence ha plan hos s can show p e e ence owa d mo e bene icial ungal axa [14–16], i may be p esumed ha such pa ne selec ion would lead o AM ungal assemblages ha con e g ea e unc ional bene i s o he hos plan com- pa ed o communi ies assembled in a pu ely s ochas ic man- ne . Based on his assump ion, i is easonable o expec ha newly assembled AM ungal communi ies, such as in oo s o seedlings, would become inc easingly phylogene ically * Adam F ew a. ew@wes e nsydney.edu.au * Ca los A. Aguila -T igue os ca los.a.aguila - igue [email p o ec ed] 1 Hawkesbu y Ins i u e o  heEn i onmen , Wes e n Sydney Uni e si y, Hawkesbu y Campus, Locked Bag 1797, Pen i h2751, NSW, Aus alia 2 Cen e o C op Heal h, Uni e si y o Sou he n Queensland, Toowoomba4350, QLD, Aus alia 3 Depa men o Biological andEn i onmen al Sciences, Uni e si y o Jy äskylä, P.O. Box35, Jy äskylänyliopis oFI-40014, Finland A.F ew, C.A.Aguila -T igue os 139 Page 2 o 8 clus e ed o e ime as hos - ungal compa ibili y is op imised o maximise symbio ic bene i s. The speci ic mechanisms h ough which hos plan s in lu- ence he assembly o AM ungal communi ies, pa icula ly in e ms o selec ing axa, emain poo ly unde s ood. Hos a ini y can be examined using di e en app oaches such as he assessmen o di e en ial ca bon alloca ion by hos s o mo e bene icial ungi [16], di ec measu emen s o plan i - ness in esponse o speci ic AM ungal axa [17], o h ough comp ehensi e sampling o mul iple hos species wi hin a gi en egion [11]. While such s udies canhighligh ha hos p e e ence could be a po en ial d i e o communi y compo- si ion, a challenge emains in consis en ly iden i ying which ungal axa p o ide he g ea es bene i s o hei hos s. This challenge is compounded by he con ex -dependen na u e o symbio ic ou comes, leading o signi ican a iabili y in he unc ional oles o di e en AM ungal lineages [18, 19]. Assigning speci ic unc ional cha ac e is ics o di e - en AM ungal axa, pa icula ly in e ms o he po en ial ‘bene i s’ hey p o ide o hos s, has p o en challenging in i sel due o he highly con ex -dependen na u e o hese ou comes [5] and he di icul ies o measu ing ai s on ungal indi iduals [20]. Despi e decades o esea ch, da a associa ing pa icula AM ungal lineages wi h speci ic sym- bio ic e ec s on plan pe o mance, emain limi ed [5, 21]. No wi hs anding his a iabili y, i is gene ally accep ed ha AM ungi exhibi phylogene ic niche conse a ism [22], ha species e ain ecological ai s and niches o e ime. Con- sequen ly, closely ela ed AM ungal axa end o exhibi simila cha ac e is ics, which could be an icipa ed o esul in simila symbio ic e ec s on a gi en hos [22]. Al hough AM ungal communi y composi ion signi i- can ly in luences symbio ic ou comes o hos plan s [3, 5], and empo al dynamics ha e been obse ed in AM ungal spo e popula ions and oo colonisa ion [23, 24], compa a- i ely ew s udies ha e di ec ly in es iga ed he empo al dynamics o AM ungal communi y composi ion wi hin plan oo s [10]. Those s udies which ha e examined his, epo signi ican changes in communi y composi ion o e ime [25–29] (bu see [30]), o en linked o hos de el- opmen al s ages o shi s in edaphic a iables. The mos de ailed o hese s udies obse ed a shi om s ochas ic o de e minis ic assembly p ocesses, wi h oo communi ies exhibi ing inc eased phylogene ic clus e ing h ough ime [25]. This was a ibu ed o he expanding a ailable habi- a — he g owing oo sys em— acili a ing he immig a ion o ungal axa wi h simila ecological niche equi emen s, esul ing in communi ies composed o mo e closely ela ed ungi. Despi e being conduc ed in a ela i ely homogene- ous ag icul u al con ex , his s udy would ne e heless ha e been in luenced by soil he e ogenei y and he na u al spa ial a ia ion in he esiden soil AM ungal communi ies, as well as po en ial dispe sal e ec s. Consequen ly, addi ional da a a e equi ed o enhance ou unde s anding o he em- po al dynamics o AM ungal communi ies in plan oo s. I also emains unclea whe he , o how, empo al shi s in he composi ion o phylogene ic s uc u e o oo -colonising communi ies ha e unc ional consequences in e ms o hei symbio ic e ec s on he hos . We conduc ed a glasshouse po expe imen wi h 60 indi- idual plan s o So ghum bicolou L. Moench c . ‘MR. Bazley’ wi h he objec i es o (i) cha ac e ising empo al changes in AM ungal communi y composi ion and phylo- gene ic di e si y wi hin plan oo s, and (ii) de e mining how hese empo al changes ela e o plan g ow h and phospho- us up ake (see Supplemen a y In o ma ion o me hodo- logical de ails). We hypo hesised ha (i) communi ies would become mo e phylogene ically clus e ed o e ime and (ii) his would co ela e wi h an inc ease in he g ow h and phos- pho us bene i s p o ided by he symbiosis o he hos . Plan s we e cul i a ed in a ully homogenised and gamma-i adia ed sand-soil mix u e, which was ei he inocu- la ed wi h a homogenised di e se communi y o AM ungi (AM ungi ea men ) o wi h a s e ilised inoculum o he same (No AM ungi ea men ). The AM ungal communi y was sou ced om a combina ion o ield soils collec ed om a ious ag icul u al and non-ag icul u al si es p e iously known o suppo a high di e si y o AM ungi (Fig.S5a). Plan s we e ha es ed a 4, 8, and 12 weeks ( imepoin s one, wo, and h ee, espec i ely), whe e 20 eplica e plan s (10 wi h AM ungi and 10 wi hou ) we e ha es ed. To al bio- mass was measu ed, olia samples we e collec ed o nu i- en analysis, and oo samples we e subjec ed o Illumina amplicon sequencing using he nuclea small subuni (SSU) RNA gene o iden i y AM ungal i ual axa (VT) [31] and cha ac e ise communi y composi ion. Changes in AM ungal communi ies o e ime we e analysed using a join species dis ibu ion Bayesian amewo k, Hie a chical Modelling o Species Communi ies (HMSC; [32]). We employed his amewo k o he abili y o model mul iple species simul- aneously while accoun ing o phylogene ic ela ionships, species in e ac ions, and hie a chical da a s uc u es. Unlike classic eg ession me hods ha model species independen ly and may o e look in e -species in e ac ions, o s anda d mul i a ia e analyses ha lack species-speci ic insigh s and explici conside a ion o phylogeny, HMSC p o ides a com- p ehensi e amewo k. This allows us o pa i ion a iance among ixed e ec s (e.g., imepoin , sequencing dep h), an- dom e ec s (e.g., indi idual plan a iabili y), and phyloge- ne ic con ibu ions, o e ing deepe ecological insigh s in o he ac o s shaping he communi y han adi ional me hods. We used his app oach in combina ion wi h calcula ing be a di e si y me ics alongside phylogene ic indices [33] meas- u ing he ex en o phylogene ic clus e ing o o e dispe sion. The AM ungal communi y dynamics we e hen assessed in ela ion o plan biomass and phospho us concen a ions Inc easing Phylogene ic Clus e ing o A buscula Myco hizal Fungal Communi ies inRoo s… Page 3 o 8 139 o explo e i and how empo al AM ungal assembly was associa ed wi h symbio ic ou comes o he hos . Ou HMSC model demons a ed high disc imina ion abili y (mean AUC = 0.88), easonable accu acy (mean RMSE = 0.25), and modes explana o y powe (mean Tju ’s R2 = 0.2) o e all. The model e alua ed he occu ence o AM ungal VT ac oss he h ee imepoin s and exhibi ed s ong suppo o axon-speci ic esponses, pa icula ly owa ds he hi d ime poin (Fig.1a). O e all, he model a ibu ed 45.3% o he explained a ia ion in AM ungal occu ence o ime (Fig.1b), wi h 29.5% o he andom e ec o indi idual sam- ples. Ou model also a ibu ed 25.2% o sequencing dep h, indica ing ha he numbe o sequences gene a ed pe sample in luenced he de ec ed axa. Including sequencing dep h in ou model allows us o accoun o his in luence and imp o es ou abili y o isola e and in e p e he ue ecological pa e ns in he da a. Ou HMSC model had a no ably high phylogene ic signal (ρ = 0.84 ± 0.0037; mean ± SE), indica ing ha he phy- logene ic ela edness s ongly p edic s which AM ungal axa a e p esen a a gi en imepoin . This sugges s ha species ai s conse ed h ough e olu iona y his o y play an impo - an ole in communi y assembly o e ime [32]. Indeed, o he 36 AM ungal axa (VT) signi ican ly associa ed wi h ime- poin h ee, 35 belonged o he Glome aceae amily (Fig.1a). Fig. 1 Hie a chical Modelling o Species Communi ies (HMSC) (a) be a coe icien s indica ing posi i e (g een), nega i e (black), o no signi ican ela ionship (blank/whi e) o a buscula myco hizal (AM) ungal i ual axa (VT) esponses wi h a leas a pos e io p obabil- i y o 0.95 associa ed wi h imepoin s wo, h ee, and sampling dep h (log eadcoun ). The mean Rho (ρ) o he model, as a measu e o phylogene ic signal in species’ esponses, is shown.b The p opo ion o explained a ia ion in AM ungal VT occu ence by ime, sam- pling dep h (log eadcoun ), and he andom e ec o sample iden- i y. Phylogene ic ee colou ed by amily is shown which includes he de ec ed AM ungi ac oss all samples, he AM ungal VT in (a) and (b) a e so ed e ically acco ding o hei phylogene ic ela edness A.F ew, C.A.Aguila -T igue os 139 Page 4 o 8 Tempo al shi s in communi y composi ion e ealed high species u no e , wi h ungi om amilies such as En ophospo aceae, A chaeospo aceae, and Di e sispo- aceae p esen a ea lie imepoin s bu mos ly absen by he hi d. Co espondingly, he a ia ion in communi y composi ion among samples ( he communi y dispe sion) was lowes a he hi d imepoin (Fig.S2), e lec ing inc easing simila i y among communi ies h ough ime. The phylogene ic di e si y also exhibi ed dis inc ends, wi h s anda dised e ec sizes o mean pai wise dis ances and mean nea es axon dis ances signi ican ly dec easing om he i s o he hi d imepoin (Fig.2a, b). These mo e nega i e alues e lec a end owa ds phylogene ic clus e ing sugges ing ha , as he AM ungal communi- ies assembled o e ime, hey became composed o mo e closely ela ed axa. This pa e n is o en hough o be indica i e o communi y assembly p ocesses d i en by some o m o en i onmen al il e ing [34, 35]. Al hough abio ic ac o s would ha e a ec ed he ou - comes obse ed in his expe imen , he homogenisa ion o he ini ial s a ing AM ungal communi y and he use o con- olled en i onmen al condi ions would ha e signi ican ly lessened hei in luence. A he e y leas , phylogene ic clus e ing unde such condi ions implies ha he closely ela ed ungal axa may sha e pa icula ai s ha hen con- e membe ship and dominance o communi ies a he la e s ages o communi y assembly. I may u he sugges ha hese ai s a e selec ed o by he plan hos , and his selec- ion d i es he success o hese axa in he sys em. I his is he case, we migh expec he hos selec ion o con e a Fig. 2 Phylogene ic di e si y o oo -colonising a buscula myc- o hizal (AM) ungal communi- ies as s anda dised e ec sizes (SES) o (a) he mean pai wise dis ances and (b) mean nea es axon dis ances a imepoin s one, wo, and h ee. The (c) myco hizal g ow h esponses (%), calcula ed using o al plan biomass, and he (d) myco hi- zal phospho us esponses (%) a each imepoin . Solid poin s and e o ba s ep esen he mean± SE o e laid on op o he aw da a poin s Inc easing Phylogene ic Clus e ing o A buscula Myco hizal Fungal Communi ies inRoo s… Page 5 o 8 139 unc ional bene i . Ou da a suppo his hypo hesis, as we ound phylogene ic clus e ing co esponded wi h posi i e plan esponses, e lec ing unc ional ad an ages (Figs.2, 3). The o al plan biomass and phospho us bene i s con- e ed by AM ungi, as e lec ed in myco hizal g ow h esponses (Fig.2c) and myco hizal phospho us esponses (Fig.2d), e ealed ha plan s de i ed li le g ow h o nu ien ad an ages om he AM ungi du ing he i s and second imepoin s. A he hi d imepoin , howe e , plan s displayed signi ican ly enhanced g ow h and phospho us up ake in esponse o AM ungi (Fig.2c, d). This coin- cided wi h he s ong posi i e associa ions o Glome aceae axa wi h imepoin h ee (Fig.1a) and he phylogene ic clus e ing o he ungal communi ies. Addi ionally, a his imepoin , a no able inc ease in he p opo ion o a buscule s uc u es wi hin oo s was also obse ed (Fig.S4d). Since a buscules a e he p ima y ungal s uc u es in ol ed in nu ien and ca bon exchange be ween he hos and ungi Fig. 3 Rela ionships be ween phylogene ic di e si y (showing he s anda dised e ec sizes, SES) o oo -colonising a buscula myc- o hizal (AM) ungal communi ies and plan hos esponses o AM ungi. The ela ionships be ween myco hizal g ow h esponses (%) and he (a) mean pai wise dis ances (MPD) and (b) mean nea es axon dis ances (MNTD), and he ela ionships be ween he myco - hizal phospho us esponses (%) and he (c) mean pai wise dis ance and he (d) mean nea es axon dis ances. Each plo shows he amoun o a ia ion in he myco hizal g ow h esponses (a, b) and myco - hizal phospho us esponses (c, d) explained by he imepoin alone, he phylogene ic di e si y (MPD o MNTD) alone, o sha ed by bo h imepoin and phylogene ic di e si y. The coe icien s o de e mina- ion (R2) showing he o al a ia ion explained (including bo h ime- poin and phylogene ic di e si y as explana o y a iables), a e shown on each plo A.F ew, C.A.Aguila -T igue os 139 Page 6 o 8 [2], a shi owa ds inc eased a buscula colonisa ion may sugges an enhanced ans e o esou ces be ween he symbio ic pa ne s. Howe e , we acknowledge ha a bus- cule equency, which can luc ua e signi ican ly o e ime [2], can be a coa se measu e o symbio ic unc ion. I is no ewo hy ha ou esul s demons a e a clea inc ease in he dominance o Glome aceae axa wi hin communi ies o e ime (Fig.1a). Glome aceae a e o en cha ac e ised as pu a i ely ude al and dis u bance- ole an ungi ha a e as -g owing, and compa a i ely less nu i- ionally bene icial o hos s han o he slowe -g owing un- gal axa [18, 36]. As ude als, hese AM ungi would be expec ed o colonise new habi a s ea ly; ye he e we ound hei dominance la e in communi y de elopmen . As such, i is less likely he s ong succession pa e ns we obse ed a e explained by phylogene ically ela ed ungal ai s ha simply allow hem o g ow as e and access he oo , bu a he ha hei sha ed ai s con ibu e o be e hos - ungal compa ibili y. Tha said, i emains possible ha hese ungi may simply possess ce ain ai s, sha ed among phylogene ically simila axa, ha allow hem o mo e eas- ily colonise his oo sys em. S ill, he s ong associa ion be ween phylogene ic clus e ing and unc ional plan ben- e i s sugges s ha hos selec ion is a s onge in luence o assembly h ough ime han passi e colonisa ion. The ude al cha ac e is ics o Glome aceae axa may indeed make hem mo e sui able symbio ic pa ne s o an ag icul u al c op selec i ely b ed o ha e as g ow h a es, pa icula ly he e in he con ex o a po expe imen which inhe en ly ep esen s a signi ican dis u bance [37, 38]. I is also impo an o no e ha assigning li e his o y s a e- gies o pa icula AM ungal lineages s ill emains augh wi h unce ain y [20] as comp ehensi e ai da a ac oss AM ungal axa a e s ill lacking. Al hough some s udies sugges ha ce ain AM ungal g oups may exhibi dis inc sui es o ai s [19, 39], con iden ly assigning lineages o a pa icula li e his o y s a egy is s ill p ema u e. We ound s ong ela ionships be ween he phylogene ic clus e ing o AM ungal communi ies and he g ow h and phospho us bene i s con e ed by he symbiosis (Fig.3). Bo h mean pai wise dis ances and mean nea es axon dis- ances exhibi ed signi ican and s ong co ela ions wi h myco hizal g ow h and phospho us esponses. Va iance pa i ioning e ealed ha he amoun o a ia ion in myco - hizal g ow h esponses explained by phylogene ic di e si y alone eached as high as 26% ( o mean pai wise dis ances), whe eas ime alone accoun ed o only 3% (Fig.3a). While he amoun o explained a ia ion in myco hizal g ow h and phospho us esponses a ied (Fig.3a-d), he imepoin alone did no explain mo e han 22% o plan esponses in any gi en ins ance. These esul s p o ide e idence ha he empo al phylogene ic clus e ing o AM ungal communi ies wi hin plan oo s can be a key d i e o he unc ional bene i s he hos de i es om he symbiosis. Ou esul s indica e ha selec i e p ocesses in he oo s can lead o posi i e ou comes o he hos plan . Howe e , we wan o s ess ha s ong hos selec ion does no nec- essa ily lead o posi i e ou comes. Fo example, e idence om plan -soil eedback expe imen s show ha hos s can os e AM ungal communi ies ha a e bene icial [40, 41] bu also communi ies ha can nega i ely impac conspe- ci ic plan s [42]. Thus, he na u e o hese in e ac ions is highly con ex dependan , bo h on he e ec o he AM ungal communi ies on he hos [5], and he deg ee o hos in luence on AM ungal communi y assembly in oo s. Since ou s udy ocuses on a single c op species, u u e esea ch should assess he empo al assembly o oo -col- onising AM ungi ac oss a wide ange o hos plan s, no only ac oss key ag icul u al species bu also na i e plan s. Unde s anding he capaci y o c ops o shape he assembly o bene icial AM ungal communi ies is essen ial o ully ha nessing he unc ional bene i s o his symbiosis. Supplemen a y In o ma ion The online e sion con ains supplemen- a y ma e ial a ailable a h ps:// doi. o g/ 10. 1007/ s00248- 024- 02457-1. Au ho Con ibu ions A.F. conduc ed he expe imen and collec ed he da a. A.F. and C.A.A-T. analysed and in e p e ed he da a. A.F. and C.A.A-T. co-w o e he manusc ip . Funding Open Access unding p o ided by Uni e si y o Jy äskylä (JYU). This wo k was suppo ed by an Aus alian Resea ch Council Disco e y Ea ly Ca ee Resea che Awa d o A.F (DE220100479). The wo k was also suppo ed by a Visi ing Fellowship G an om he Uni e si y o Jy äskylä awa ded o A.F. CAA-T was suppo ed by an Academy Resea ch Fellowship (21000058691) om he Resea ch Council o Finland (Suomen Aka emia). Da a A ailabili y Da a ha suppo his s udy a e openly a ailable om he Figsha e eposi o y a he ollowing doi: h ps:// doi. o g/ 10. 6084/ m9. igsh a e. 26928 256, which will become li e upon a icle publica- ion. Raw DNA sequencing da a a e a ailable unde NCBI BioP ojec accession numbe PRJNA1156093. Decla a ions Compe ing In e es s The au ho s decla e no compe ing in e es s. Open Access This a icle is licensed unde a C ea i e Commons A i- bu 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. 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