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In eg a ing Decompose s, Me hane-Cycling Mic obes and Ecosys em Ca bon Fluxes
Along a Pea land Successional G adien in a Land Upli Region
© Au ho s, 2021
Published e sion
Juo onen, Heli; Kieman, Mi kka; F i ze, Hannu; Hambe g, Leena; Laine, Anna M.;
Me ilä, Päi i; Pel oniemi, K is a; Pu kinen, Anuliina; Tui ila, Ee a-S iina
Juo onen, H., Kieman, M., F i ze, H., Hambe g, L., Laine, A. M., Me ilä, P., Pel oniemi, K.,
Pu kinen, A., & Tui ila, E.-S. (2022). In eg a ing Decompose s, Me hane-Cycling Mic obes and
Ecosys em Ca bon Fluxes Along a Pea land Successional G adien in a Land Upli Region.
Ecosys ems, 25(6), 1249-1264. h ps://doi.o g/10.1007/s10021-021-00713-w
2022
In eg a ing Decompose s, Me hane-
Cycling Mic obes and Ecosys em
Ca bon Fluxes Along a Pea land
Successional G adien in a Land
Upli Region
Heli Juo onen,
1,2
* Mi kka Kieman,
3
Hannu F i ze,
4
Leena Hambe g,
4
Anna M. Laine,
3,5,6
Pa
¨i i Me ila
¨,
7
K is a Pel oniemi,
4
Anuliina Pu kinen,
2,8,9
and Ee a-S iina Tui ila
3,6
1
Depa men o Biological and En i onmen al Science, Uni e si y o Jy a
¨skyla
¨, P.O. Box 35, 40014 Jy a
¨skyla
¨, Finland;
2
Depa men o
Biosciences, Gene al Mic obiology, Uni e si y o Helsinki, P.O. Box 56, 00014 Helsinki, Finland;
3
Pea land Ecology G oup, Depa -
men o Fo es Sciences, Uni e si y o Helsinki, P.O. Box 27, 00014 Helsinki, Finland;
4
Na u al Resou ces Ins i u e Finland (Luke),
P.O. Box 2, 00791 Helsinki, Finland;
5
P esen Add ess: Geological Su ey o Finland, Neulaniemen ie 5, P.O. Box 1237, 70211 Kuopio,
Finland;
6
P esen Add ess: School o Fo es Sciences, Uni e si y o Eas e n Finland, P.O. Box 111, 80101 Joensuu, Finland;
7
Na u al
Resou ces Ins i u e Finland (Luke), Paa o Ha aksen ie 3, 90570 Oulu, Finland;
8
En i onmen al Soil Science, Depa men o Ag i-
cul u e, Uni e si y o Helsinki, P.O. Box 56, 00014 Helsinki, Finland;
9
Ins i u e o A mosphe ic and Ea h Sys em Resea ch (INAR)/
Fo es Sciences, Uni e si y o Helsinki, P.O. Box 56, 00014 Helsinki, Finland
ABSTRACT
Pea lands a e ca bon dioxide (CO
2
) sinks ha , in
pa allel, elease me hane (CH
4
). The pea land ca -
bon (C) balance depends on he in e play o
decompose and CH
4
-cycling mic obes, ege a ion,
and en i onmen al condi ions. These in e ac ions
a e suscep ible o he changes ha occu along a
successional g adien om ascula plan -domi-
na ed sys ems o Sphagnum moss-domina ed sys-
ems. Changes simila o his succession a e
p edic ed o occu om clima e change. He e, we
in es iga ed how mic obial and plan communi ies
a e in e linked wi h each o he and wi h ecosys em
C cycling along a successional g adien on a bo eal
land upli coas . The g adien anged om sho e-
line o meadows and ens, and u he o bogs.
Po en ial mic obial ac i i y (ae obic CO
2
p oduc-
ion; CH
4
p oduc ion and oxida ion) and biomass
we e g ea es in he ea ly successional meadows,
al hough hei communi ies o ae obic decom-
pose s ( ungi, ac inobac e ia), me hanogens, and
me hano ophs did no di e om he olde ens.
Ins ead, he unc ional mic obial communi ies
shi ed a he en–bog ansi ion concu en wi h a
sudden dec ease in C luxes. The successional pa -
e ns o decompose e sus CH
4
-cycling commu-
ni ies di e ged a he bog s age, indica ing s ong
bu dis inc mic obial esponses o Sphagnum
dominance and acidi y. We highligh young
meadows as dynamic si es wi h he g ea es
mic obial po en ial o C elease. These ho spo s o
C u no e wi h dense sedge co e may ep esen a
Recei ed 5 May 2021; accep ed 16 Sep embe 2021
Supplemen a y In o ma ion: The online e sion con ains supple-
men a y ma e ial a ailable a h ps://doi.o g/10.1007/s10021-021-0071
3-w.
EST and HF concei ed he s udy; EST, PM and AML pe o med ield
sampling and lux measu emen s; MK, HJ, KP and AP pe o med esea ch
in he lab; LH, MK, AML and HJ analyzed da a; HJ, MK, HF, AML, LH and
EST w o e he pape and all au ho s commen ed on i .
*Co esponding au ho ; e-mail: heli.[email p o ec ed]
Ecosys ems
h ps://doi.o g/10.1007/s10021-021-00713-w
2021 The Au ho (s)
sensi i e bo leneck in succession, which is neces-
sa y o e en ual long- e m pea accumula ion. The
dis inc i e mic obes in bogs could se e as indica-
o s o he C sink unc ion in es o a ion measu es
ha aim o s abilize he C in he pea .
Key wo ds: ecosys em espi a ion; me hane
emission; ungi; ac inobac e ia; me hanogens;
me hano ophs; mic obial biomass; mic obial
communi y; p ima y paludi ica ion; pea land
de elopmen .
HIGHLIGHTS
Ea ly successional meadows we e ho spo s o
mic obial ac i i y and ca bon u no e .
Mic obial communi y shi ed a he en–bog
ansi ion wi h dec easing ca bon lux.
Mic obes in bogs could be indica o s o he
ca bon sink unc ion o a pea land.
INTRODUCTION
Abou 30% o he global soil ca bon (C) is s o ed in
pea lands (Go ham 1991). Consequen ly, pea land
ecosys ems play a key ole in con olling a mo-
sphe ic ca bon dioxide (CO
2
) and me hane (CH
4
)
concen a ions (Yu 2012). They a e unique habi a s
o la gely wa e -logged o ganic soils, whe e chan-
ges in en i onmen al condi ions a ec he in e play
o p ima y p oduce s and decompose s, which can
u n he sys em in o a C sink o sou ce ( o
example, Laiho 2006). This in e play includes
plan s, ungi, bac e ia, and CH
4
-p oducing a chaea
(me hanogens) and CH
4
-oxidizing bac e ia (MOB)
especially, which a e p esen unde speci ic en i-
onmen al condi ions ha a e de e mined by
mois u e con en and e ili y le el (So oco nola
and o he s 2009; Ande sen and o he s 2011,2013).
Clima e change is likely o dis up he complex
in e play ha de e mines he pea land C balance.
In pea lands, he impac s o wa ming a e expec ed
o be coupled wi h d ying due o inc eased e apo-
a ion (Roule and o he s 1992; Monie and o he s
2013; Helbig and o he s 2020). Wa ming and d y-
ing a e ad an ageous o he ac i i y o mos
decompose s, he eby inc easing he a es o min-
e aliza ion ( o example, Dieleman and o he s
2016). In addi ion, he communi y composi ion
esponds o en i onmen al changes: ascula plan s
ha e an ad an age o e Sphagnum mosses in wa -
me and d ie condi ions (Wel zin and o he s 2000;
B eeuwe and o he s 2009; Dieleman and o he s
2015). The communi y esponse o ungi, ac i-
nobac e ia, me hanogens, and MOB o wa ming
and d ying appea s o depend on pea land e ili y
(Jaa inen and o he s 2005; Pel oniemi and o he s
2009,2015,2016; U bano a
´and Ba
´ a 2016). Such
communi y changes ha e been linked wi h al e -
a ions in se e al ecosys em unc ions, such as de-
c eased C accumula ion (Riu a and o he s 2007;
B agazza and o he s 2016; Laine and o he s 2019b)
and inc eased decomposi ion o o ganic ma e
(S ako a
´and o he s 2012). In gene al, d ying
appea s o ha e a s onge impac on pea land
communi ies and unc ions han wa ming (Pel-
oniemi and o he s 2016;Ma
¨ki an a and o he s
2018; Laine and o he s 2019a,2019b). Al hough
he esponses o indi idual communi ies (plan s o
mic obes) o en i onmen al changes ha e been
s udied o some ex en , e y ew s udies ha e
linked he concu en esponses o mul iple com-
muni ies o ecosys em unc ions, such as CO
2
and
CH
4
exchange (howe e , see Jassey and o he s
2013,2018; Rob oek and o he s 2015).
No he n pea lands a e dynamic sys ems ha
ypically ha e unde gone succession om ascula -
domina ed o Sphagnum moss-domina ed sys ems
du ing hei de elopmen ( o example, Baue and
o he s 2003). Simila apid di ec ional change has
been epo ed as a esponse o al e ed hyd ology as
pa o clima e change (Gunna sson and o he s
2002; Tah anainen 2011). Concu en wi h he
plan communi y, he mic obial communi ies also
unde go successional change (Me ila
¨and o he s
2006; Pu kinen and o he s 2014). Pea land p ima y
succession leads o changes in ecosys em unc ions,
such as CO
2
and CH
4
exchange (Leppa
¨la
¨and o he s
2008,2011a,2011b). P ima y succession g adien s
make i possible o assess how igh ly he di e en
communi ies a e linked and o p edic changes in
mic obial composi ion based on he change in plan
communi y s uc u e. Pea land ch onosequences a
land upli coas s (Glase and o he s 2004; Tui ila
and o he s 2013; Ha is and o he s 2020; Laine and
o he s 2021) o e excellen se ings o s udy how
he communi y changes a e in e linked wi h
ecosys em unc ions, as communi ies and unc ions
can be s udied unde simila clima ic and wea he
condi ions.
The aim o his s udy was (1) o quan i y how
successional pa e ns in di e en unc ional g oups
(plan s, ungi, ac inobac e ia, me hanogens, MOB)
a e in e linked, and (2) o link he change in
communi ies wi h he change in ecosys em unc-
ions (CO
2
p oduc ion po en ial, CH
4
p oduc ion
H. Juo onen and o he s
and oxida ion po en ial, ecosys em espi a ion, CH
4
emissions). We expec ed ha as b oad g oups o
ae obic li e decompose s, ungi and ac inobac e ia
succession would closely ollow ha o ege a ion
because li e ype appea s o be a mo e impo an
de e minan o ungal and ac inobac e ial com-
muni ies in bo eal pea lands han hyd ology (Pel-
oniemi and o he s 2009,2012). Me hanogens and
MOB, on he o he hand, we e expec ed o ollow
he posi ion o he wa e le el (WL), which con ols
he ae a ion o he pea (U bano a
´and o he s
2011;Y ja
¨la
¨and o he s 2011), as well as he
p e alence o sedges and Sphagnum mosses, which
a e subs a e sou ces and habi a s o CH
4
-cycling
mic obes, espec i ely (S o
¨m and o he s 2003;
Pu kinen and o he s 2014).
MATERIALS AND METHODS
S udy Si es
The s udy a ea is loca ed on he Finnish coas o he
Gul o Bo hnia (6445¢N, 2442¢E), whe e new
land is exposed om he sea due o pos -glacial
isos a ic ising. On a 10-km ansec ha ex ends
om he sho e inland, he si es comp ise se en
nea na u al pea lands (SJ0–SJ6), wi h successional
s ages ha anged om he onse o p ima y pea
o ma ion o a bog s age, which is conside ed as he
inal s age o succession (Table 1, Figu e S1). The
ea ly s ages (SJ0–SJ2) ha e a a he la su ace,
while in he la e s ages (SJ3–SJ6) he pea land
su ace is pa e ned by mic o o ms (d y aised
hummocks, in e media e lawns, we la ks wi h
pea su ace a o below wa e le el (WL)). Typical
mic o o ms we e lawns (Sphagnum co e ed) and
la ks in SJ3 and SJ4, hummocks, lawns and la ks
in SJ5, and sh ubby hummocks, hummocks, and
lawns in SJ6.
Field Measu emen s
F om June o Sep embe 2007, CH
4
and CO
2
luxes
(ecosys em espi a ion, RE) we e measu ed a
weekly o biweekly in e als om 54 pe manen
sample plo s (0.56 m 90.56 m) es ablished o
co e he si e-speci ic a ia ion in ege a ion (Ta-
bles 1and S1). Gas luxes we e measu ed wi h he
s a ic chambe me hod (see supplemen a y ma e-
ial o de ails). Wa e le el and pea empe a u e
a 5, 10, and 20 cm dep hs we e measu ed close o
each plo du ing he lux measu emen s. Plan
species co e was in en o ied om he same plo s
a he end o July 2007 (Table S1). Pe cen age
co e o ascula and moss species was es ima ed
isually using he scale 0.25, 0.5, 1, 2, 3–100%.
Pea Sampling and Physicochemical
Analyses
In Augus 2007, we collec ed wo pa allel se s o
soil co es (one o mic obiological and one o
physicochemical analysis) wi h a box sample
(8 989100 cm) o wi h a cylinde sample
(4.5 cm diame e , 50 cm leng h) om each si e
along he ansec . The co es we e aken wi hin
2 m o each gas lux sample plo om a eas wi h
simila ege a ion o a oid dis u bance on he plo s.
In addi ion o he si es wi h gas lux measu emen s
(SJ0–SJ6), we ook ou co es om he sandy
subme ged li o al zone (SJm1) nea SJ0 o ep e-
sen he soil be o e he land was exposed.
Table 1. Cha ac e is ics o Successional S ages Along he Pea land G adien
Si e Successional
s age
Te es ial age
(y)
a
Pea hickness
(cm)
a
Typical ege a ion Numbe o sample
plo s
SJm1 Unde he sea
le el
0 0 Ph agmi es 4
SJ0 Exposed sho e 70 0 G asses 6
SJ1 Epilobium mea-
dow
100–180 £10 G asses, sedges, b own mosses 6
SJ2 Equise um mea-
dow
150–200 £10 G asses, sedges, b own mosses 6
SJ3 Meso ophic en 500–700 50 Sedges, Sphagnum sp. 10
SJ4 Oligo ophic en 1070 ±70 75 Sedges, sh ubs, Sphagnum sp. 9
SJ5 Fen–bog ansi-
ion
2520 ±50 180 Sedges, sh ubs, Sphagnum sp., S.
uscum
8
SJ6 Bog 3000 170–230 Sh ubs, S. uscum 9
a
The alues o e es ial age and pea hickness a e summa ized om Me ila
¨and o he s (2006) and Leppa
¨la
¨and o he s (2008).
Mic obes and C Fluxes in Pea land Succession
The sampling p ocedu e co e ed he a ia ion in
mois u e and ege a ion ypical o each si e. The
co es (n= 58), which eached dep hs o 30, 45, o
60 cm, we e cu a e en in e als (10, 15, o
20 cm) esul ing in h ee pea laye s: uppe mos ,
middle, and deepes laye (174 samples in o al).
The leng h o he in e al depended on he pea
dep h and WL: longe sec ions we e used o si es
wi h deepe pea and WL. Va ying he in e al
( ha is, hickness o he h ee pea laye s) allowed
us o co e he pea abo e, a ound and below WL
a each si e despi e hei widely di e en pea
dep hs (Table 1). Po ions o he samples we e used
o measu ing pH (soil:wa e 1:5 / ) and o
de e mine he po en ial a es o CO
2
and CH
4
p oduc ion and CH
4
oxida ion. The emainde o
he samples we e ozen (-20 C) o molecula
and phospholipid a y acid (PLFA) analyses. Pa -
allel olume ic soil co es we e used o de e mine
bulk densi y, o ganic ma e (OM; loss in weigh on
igni ion, 500 C, 4 h), and o al C and ni ogen (N;
LECO CHN-2000 analyze ). Resul s we e calcula ed
by olume based on he bulk densi y o he olu-
me ic sample slices (g dm
-3
).
Po en ial CO
2
P oduc ion, CH
4
P oduc ion, and CH
4
Oxida ion
Po en ial ac i i y measu emen s o he h ee pea
laye s (uppe mos , middle, deepes ) we e ca ied
ou in 120-ml lasks wi h 15 ml o pea (see sup-
plemen a y ma e ial o u he de ails). The lasks
o CH
4
p oduc ion con ained 30 ml o wa e and
we e lushed wi h ni ogen. The lasks o CH
4
oxida ion ecei ed 100 llo CH
4
as subs a e. The
lasks we e incuba ed a 15 C in he da k o
4 days (CH
4
p oduc ion) o 1–2 days (CO
2
p o-
duc ion and CH
4
oxida ion). Gas concen a ions
we e ollowed by gas ch oma og aphy as desc ibed
in Pe kio
¨ma
¨ki and F i ze (2002; ae obic CO
2
p o-
duc ion), Jaa inen and o he s (2005;CH
4
oxida-
ion), and Me ila
¨and o he s (2006;CH
4
p oduc ion). P oduc ion o oxida ion a es we e
calcula ed om he slope o he linea eg ession o
gas concen a ion change o e ime. The a es a e
gi en pe sample olume (mg o lgdm
-3
h
-1
).
Phospholipid Fa y Acid (PLFA)
Analysis
Fungal and bac e ial biomass was analyzed by
quan i ying PLFAs om 1.5 o 4 g we weigh o
pea o 4–6 g we weigh o mine al soil (F os ega
˚ d
and o he s 1993; Jaa inen and o he s 2007). Rela-
i e ungal abundance (F-PLFA) was quan i ied
om he amoun o PLFA 18:2x6 (F os ega
˚ d and
Ba
˚a
˚ h 1996; Kaise and o he s 2010). The sum o
wel e PLFAs (i15:0, a15:0, 15:0, i16:0, 16:1x9,
16:1x7 , i17:0, a17:0, 17:0, cy17:0, 18:1x7 and
cy19:0) was conside ed o ep esen bac e ial
abundance (B-PLFA) (F os ega
˚ d and Ba
˚a
˚ h 1996).
PLFAs 10Me17 and 10Me18 we e conside ed o
ep esen ac inobac e ia (Ac -PLFA) (K oppens ed
1985). The quan i y o he PLFAs was de e mined
in ela ion o he sample olume (lmol dm
-3
)by
calcula ing he esul s pe d y weigh (lmol g
-1
)
and mul iplying wi h he sample-speci ic bulk
densi y (g dm
-3
).
Molecula Analyses o Mic obial G oups
To al DNA was ex ac ed om he soil wi h a Powe
Soil DNA ex ac ion ki (MoBio Labo a o ies, Inc.,
Ca lsbad, CA, USA). Fungi we e ampli ied wi h
p ime s ITS1F and ITS2 o he in e nal ansc ibed
space egion (Ga des and B uns 1993). Ac i-
nobac e ial p ime s we e S-C-Ac -0235-a-S-20 and
S-C-Ac -0878-a-A-19 o ac inobac e ial 16S ibo-
somal RNA gene (S ach and o he s 2003). Type II
me hano ophs ( II-MOB) we e de ec ed wi h p i-
me s A189 and A621 (Holmes and o he s 1995;
Tuomi i a and o he s 2009) o me hano oph-
speci ic pmoA gene o pa icula e me hane
monooxygenase. Me hanogens we e de ec ed wi h
he p ime s o Lu on and o he s (2002) ha am-
pli y me hanogen-speci ic mc A gene o me hyl-
coenzyme M educ ase. Fungal, ac inobac e ial,
and ype II MOB communi ies we e analyzed by
dena u ing g adien gel elec opho esis (DGGE)
and sequencing o DGGE bands. Me hanogens
we e analyzed by e minal agmen leng h poly-
mo phism (T-RFLP) and sequencing o clones. The
de ails o PCR, DGGE, and T-RFLP a e desc ibed in
he supplemen a y ma e ial. The DGGE banding
pa e ns o ungi, ac inobac e ia, and II-MOB we e
compiled in o p esence-absence ma ices. DGGE
bands wi h di e gen mobili y we e conside ed as
ope a ional axonomic uni s (OTUs). Fo me ha-
nogens, T-RFs o di e en leng hs we e conside ed
as OTUs and ela i e peak a eas we e used as el-
a i e abundances. The OTUs ha appea ed a leas
wice in a da ase we e included in he communi y
composi ion da a. To de e mine axonomic a ilia-
ions, we cons uc ed phylogene ic ees o DGGE
band sequences ( ungi, ac inobac e ia, II-MOB)
and clone sequences (me hanogens; see supple-
men a y ma e ial o de ails). DNA sequences we e
submi ed o he Eu opean Nucleo ide A chi e
unde accession numbe s LN681001-LN681094
( ungi), LN681095-LN681133 (ac inobac e ia),
H. Juo onen and o he s
LN681148-LN681172 ( II-MOB), and LR999478-
LR999518 and HG993108-HG993123 (me hano-
gens).
S a is ical Analyses
The e ec s o soil p ope ies on po en ial mic obial
ac i i ies and biomass we e in es iga ed using
gene alized addi i e mixed models (GAMMs) in
package mgc wi h unc ion gamm (Wood 2006)in
R ( . 3.1.1, R Co e Team 2014). No mal dis ibu-
ion was assumed bu esponse a iables we e log-
ans o med when needed o achie e no mali y.
All sample plo s in SJ0–SJ6 we e included in he
analyses (n= 54). Models we e es ima ed sepa-
a ely o each soil laye . Because many o he
a iables ha desc ibe soil p ope ies we e s ongly
co ela ed (Table S2), only he mos impo an
( ha is, WL, OM, and pH) we e included in he
models. Wa e le el, as he mean o he measu e-
men s up o he sampling da e, was included in he
model as a ca ego ical a iable wi h alues 0 ( he
e ical middle poin o a sample below he mean
WL) and 1 ( he e ical middle poin o a sample
abo e he mean WL). We conside ed his an
accep able es ima ion o he di e ences in he
mois u e condi ions a a a he small spa ial scale
(Figu e S2). O ganic ma e and pH we e smoo hed
when he models we e es ima ed. In addi ion o
hese ixed e ec a iables, si e was included as a
andom ac o in he models. Response cu es we e
d awn based on GAMMs using mean alues o he
o he explana o y a iables a he han hose o
in e es in he models.
Global non-me ic mul idimensional scaling
(GNMDS) was pe o med o he ege a ion and
each mic obial g oup o in es iga e changes in
hese communi ies along he successional g adien ,
using he egan package ( . 2.3-0, Oksanen and
o he s 2015) in R. The B ay–Cu is dissimila i y
measu e was used o ege a ion (co e da a),
Raup–C ick o ungi, ac inobac e ia and II-MOB
(bina y da a), and Gowe o me hanogens (nu-
me ic da a). Sepa a e Me aMDS uns we e pe -
o med 50 imes o ensu e he bes possible solu ion
( ha is, o a oid local op ima). The solu ion wi h
he lowes s ess alue was chosen. En i onmen al
a iables we e i ed using pe mu a ion es s. Spe-
cies ha occu ed in a leas in i e samples we e
d awn o species o dina ion igu es. The e ec o
successional s age and pea laye on mic obial
communi ies was es ed wi h pe mu a ional anal-
ysis o a iance (PERMANOVA) (Ande son 2001)
wi h he unc ion adonis2 in he egan package.
P oc us es analysis wi h he unc ions p oc us es
and p o es in he egan package based on he i s
ou NMDS dimensions was used o compa e he
successional pa e ns o di e en unc ional g oups
(Pe es-Ne o and Jackson 2001; Lisboa and o he s
2014). The P oc us es analysis be ween ege a ion
and mic obial g oups only included he uppe mos
and middle laye s o ocus on he laye s in luenced
by he su ace ege a ion. The analyses be ween
mic obial g oups included all laye s. The dis ance
measu es in PERMANOVA and P oc us es analysis
we e he same as in GNMDS. Finally, we used he
P oc us es esiduals o compa e he s eng h o
co ela ion among mic obial g oups along he
pea land succession (Lisboa and o he s 2014). Di -
e ences be ween successional s ages we e de e -
mined wi h analysis o a iance and Tukey’s pos
hoc es s.
RESULTS
Vege a ion, Soil Chemical Va iables, Gas
Fluxes and Mic obial Biomass Along
he Pea land Succession
Along he successional g adien , o al ege a ion
co e inc eased om <20% in ecen ly exposed
sho e SJ0 o nea ly 150% in bog SJ6 (Figu e 1a,
Table S3). F om he en SJ3 onwa d, he inc easing
ege a ion co e was due o he inc ease in sh ubs
(Figu e 1b) and Sphagnum mosses (Figu e 1c).
Sedge co e was highes in he en SJ3. O ganic
ma e densi y ipled om meadow SJ2 o en SJ3,
indica ing he s a o pea accumula ion (Fig-
u e 1 ). Al hough OM, C, and N densi ies we e
g ea es in he en si es SJ3 and SJ4, C:N inc eased
h oughou he g adien (SJ0–SJ6) (Figu e 1g).
Acidi y inc eased along he g adien om pH 6.1 in
SJ0 o 4.2. in SJ6 (Figu e 1e). Wa e le el was
lowes in he bog SJ6 (Figu e 1e).
Ecosys em espi a ion peaked in en SJ3 (Fig-
u e 1d). CH
4
emissions showed a he simila le els
in si es SJ1–SJ5 and we e lowes a he end poin s
o he g adien (Figu e 1d). The g ea es mic obial
ac i i y po en ial, as indica ed by he a es o ae -
obic CO
2
and anae obic CH
4
p oduc ion, was
measu ed a he meadow si es, especially SJ2
(Figu e 1h). In con as , po en ial CH
4
oxida ion
inc eased om SJ0 o SJ2 and hen emained a
his ele a ed le el along he whole g adien . Fun-
gal, bac e ial, and ac inobac e ial biomass peaked
in he meadow si es and we e g ea es in SJ2. The
a io o ungi o bac e ia (F:B) was g ea es in he
oldes si es SJ5 and SJ6 (Figu e 1i).
Mic obes and C Fluxes in Pea land Succession
Wi hin-Si e Va ia ion in Rela ion
o Mic o o m and Pea Laye
To cap u e he p onounced e ical a ia ion and
ho izon al pa e ning ypical o bo eal pea lands,
ou sampling s a egy co e ed h ee pea laye s and
he di e en mic o o ms in he s ages whe e
mic o o ms we e p esen . The young meadow si es
SJ0–SJ2 showed no ho izon al pa e ns o ege a-
ion co e , C luxes, soil p ope ies, o mic obial
a iables. These si es had a hin o ganic su ace
laye ha co e ed he mine al soil (Table 1). Ve -
ically, his laye showed he g ea es CO
2
and CH
4
p oduc ion and CH
4
oxida ion a es and mic obial
biomass a hese si es (Table S4). In he olde si es
SJ3–SJ6 wi h hicke pea laye and mic o o ms,
he co e o Sphagnum mosses and sh ubs was
g ea e in d ie mic o o ms (lawns in SJ3 and SJ4,
hummocks in SJ5 and SJ6) (Table S5). Mic o o m-
ela ed a ia ion in RE was low, whe eas CH
4
emissions we e gene ally g ea e in he mois e
mic o o ms wi hin he si es SJ3–SJ6. Po en ial CO
2
p oduc ion in he olde si es did no a y wi h
dep h o mic o o m. Po en ial CH
4
p oduc ion in
SJ3–SJ6 was gene ally g ea e below WL and in he
mois e mic o o ms (Tables S4–S6). CH
4
oxida ion
a es we e gene ally g ea e below he uppe mos
laye , especially in he d ie mic o o ms. Fungal
Figu e 1. Va iables desc ibing pea land succession (SJ0–SJ6) wi h land upli om he sea (SJm1): a–cplan unc ional
ype co e , decosys em espi a ion (RE) and me hane (CH
4
) emissions, e–gwa e le el (WL) and soil p ope ies, h
po en ial a es o ca bon dioxide (CO
2
) (ae obic) and CH
4
p oduc ion and CH
4
oxida ion, and imic obial biomass: B-PLFA,
bac e ial phospholipid a y acids (PLFAs); F-PLFA, ungal PLFAs; Ac -PLFA, ac inobac e ial PLFAs; F:B is he a io o
ungal o bac e ial PLFAs. Values a e si e means including h ee pea laye s (SJm1 n= 12; SJ0–SJ2 n= 18; SJ3 n= 30; SJ4
n= 27: SJ5 n= 24; SJ6 n= 27). To i he scale, F:B and CH
4
emissions a e p esen ed 100 imes la ge , o ganic ma e
(OM) and ni ogen (N) 10 imes la ge , and CO
2
p oduc ion 10 imes smalle han he ini ial alues.
H. Juo onen and o he s
biomass dec eased wi h dep h in SJ3–SJ6, whe eas
bac e ial and ac inobac e ial biomass we e mainly
g ea es in he middle laye (Table S6).
Rela ionship o Mic obial Ac i i y
Po en ials o Soil Va iables Based
on Gene alized Addi i e Mixed Models
(GAMMs)
Po en ial CO
2
p oduc ion inc eased wi h inc easing
OM densi y in all laye s (Figu e 2a–c). In he
middle laye , CO
2
p oduc ion le eled a an OM
densi y o abou 70 g dm
-3
and g ea e (Fig-
u e 2b). The deepes laye showed g ea e CO
2
p oduc ion when he laye was abo e he WL
(Figu e 2c). Simila ly, po en ial CH
4
p oduc ion
was a ec ed by he posi ion o he WL (Figu e 2d–
). In he su ace laye , CH
4
p oduc ion inc eased
wi h highe pH (>5) bu only when he laye was
below he WL (Figu e 2d). In he middle laye ,
none o he selec ed soil p ope ies explained he
CH
4
p oduc ion a e, wi h he possible excep ion o
WL (p= 0.059). In he deepes laye , only a weak
link was obse ed be ween CH
4
p oduc ion and
inc easing OM densi y, bu only i his laye was
abo e he WL (Figu e 2 ). The esponse o po en ial
CH
4
oxida ion depended on he pea laye . In he
su ace laye , CH
4
oxida ion inc eased wi h
inc easing OM densi y, especially unde he WL
and a pH 5 (Figu e 2g). In he middle laye , CH
4
Figu e 2. E ec s o wa e le el (WL), o ganic ma e (OM) densi y, and pH on he mic obial ac i i y po en ials (ae obic
CO
2
p oduc ion, CH
4
p oduc ion, and oxida ion) o h ee pea laye s. Si es SJ0–SJ6 we e included in he model o each
laye (n= 54). Response cu es we e d awn based on gene alized addi i e mixed models (GAMMs) so ha explana o y
a iables o he han he p esen ed a iable we e e ained as hei mean alue. The e ec s o OM and pH a e p esen ed
only when p<0.05. All e ec s o he WL ca ego ies (abo e, below) a e shown (p alues in bold when p<0.05). Emp y
sub igu e e had no signi ican soil p ope ies. In igu es d–i: black deno es OM densi y; g ay deno es pH. No e he di e en
axis scales. R
2adj.
= adjus ed R
2
alue o he model.
Mic obes and C Fluxes in Pea land Succession
oxida ion a ied s ongly wi h OM densi y and
peaked a an OM densi y o abou 50 g dm
-3
(Figu e 2h). In he deepes laye , CH
4
oxida ion
was accen ua ed, especially abo e he WL, by
inc easing acidi y and OM (Figu e 2i).
Plan and Mic obial Communi ies Along
he Pea land G adien
Vege a ion o med a clea g adien om SJ0 o SJ6
(Figu e 3); om g ass- o sedge-domina ed com-
muni ies, and inally o Sphagnum-domina ed eg-
e a ion (including dwa sh ubs). Bulk densi y, pH,
C:N, and he co e o Sphagnum and sh ubs showed
he g ea es co ela ion ( ‡0.74) wi h plan com-
muni y change (Table S7). O e all mic obial com-
muni y s uc u e based on PLFAs showed a simila ,
hough less di e en ia ed, successional g adien
and sepa a ed he young meadows (SJ1, SJ2), mid-
successional ens (SJ3, SJ4), and he oldes bog si es
(SJ5, SJ6) om each o he (Figu e 4). A he le el
o mic obial unc ional g oups, successional s age
explained a la ge p opo ion o communi y a i-
a ion han pea laye o all he g oups (Table 2).
The communi y s uc u e o ungi, ac inobac e ia,
and me hanogens showed a common pa e n
whe e he la e s ages (SJ5, SJ6) we e sepa a ed
om he o he s ages, and he ea ly (SJ0–SJ2) and
mid-successional (SJ3, SJ4) s ages we e g ouped
oge he (Figu e 5a–i, Figu e S3). Me hano ophs
we e no de ec ed in he younges si es (SJ0, SJ1).
The II-MOB communi y in he oldes si es (SJ5,
SJ6) was sepa a ed om he younge si es, bu II-
MOB also di e ed mo e clea ly wi h pea laye
han he o he g oups (Figu e 5j–l). Changes in he
ungal, ac inobac e ial, and II-MOB communi ies
co ela ed bes wi h C:N, pH and he co e o
Sphagnum and sh ubs, and he me hanogen com-
muni ies wi h C, N, and OM densi y and Sphagnum
co e (Table S8). We used P oc us es analysis,
which supe imposes wo o dina ions, o compa e
he successional pa e ns o ege a ion and mic o-
bial unc ional g oups. Fungal communi y showed
he g ea es co ela ion wi h ege a ion composi-
ion, and ac inobac e ia he lowes (Table 2). When
compa ing he successional pa e ns o he di e en
unc ional g oups, he s onges co ela ions we e
seen be ween ac inobac e ia and ungi, and be-
ween ac inobac e ia and me hanogens, and lowes
be ween me hanogens and II-MOB (Table 2).
P oc us es esiduals showed a ai ly uni o m co -
ela ion o ac inobac e ia s. ungi and me hano-
gens s. II-MOB along he g adien (Figu e 6).
P oc us es esiduals o ac inobac e ia and ungi
wi h CH
4
-cycling mic obes inc eased owa d he
bog si es, pa icula ly he oldes si e SJ6, indica ing
dec easing co ela ion o communi y pa e ns.
Phylogene ic A ilia ion o he Mic obial
G oups
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