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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.
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Inc easing Phylogene ic Clus e ing o A buscula Myco hizal Fungal Communi ies inRoo s… Page 7 o 8 139
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