Integrating Decomposers, Methane-Cycling Microbes and Ecosystem Carbon Fluxes Along a Peatland Successional Gradient in a Land Uplift Region
Full text
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/
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
The majo i y o ungal sequences clus e ed wi h
Ascomyco a and Pezizomyco ina, including gene a
Penicillium (SJ0), A iculospo a (SJ0, SJ1, SJ4),
Figu e 3. Global non-me ic mul idimensional scaling (GNMDS) o dina ion o a ege a ion in si es SJ0–SJ6, and bplan
species sco es. O als ep esen 95% con idence in e als. The ec o s in a ep esen en i onmen al a iables wi h
co ela ion ‡0.5.
H. Juo onen and o he s
Jaa inen K, Tui ila ES, Laine J, Y ja
¨la
¨K, F i ze H. 2005. Me-
hane-oxidizing bac e ia in a Finnish aised mi e complex:
e ec s o si e e ili y and d ainage. Mic ob Ecol 50:429–439.
Jaa inen K, F i ze H, Laine J, Laiho R. 2007. E ec s o sho -and
long- e m wa e -le el d awdown on he popula ions and
ac i i y o ae obic decompose s in a bo eal pea land. Global
Change Biol 13:491–510.
Jassey VE, Chiapusio G, Bine P, Bu le A, Laggoun-De
´ a ge F,
Dela ue F, Gilbe D. 2013. Abo e-and belowg ound linkages
in Sphagnum pea land: clima e wa ming a ec s plan -mic o-
bial in e ac ions. Global Change Biol 19:811–823.
Jassey VE, Reczuga MK, Zielin
´ska M, Słowin
´ska S, Rob oek BJ,
Ma io e P, B agazza L. 2018. Tipping poin in plan – ungal
in e ac ions unde se e e d ough causes ab up ise in pea -
land ecosys em espi a ion. Global Change Biol 24:972–986.
Juo onen H. 2020. Disen angling he e ec s o me hanogen
communi y and en i onmen on pea land g eenhouse gas
p oduc ion by a ecip ocal ansplan expe imen . Func Ecol
34:1268–1279.
Juo onen H, Galand PE, Tui ila ES, Laine J, F i ze H, Y ja
¨la
¨K.
2005. Me hanogen communi ies and bac e ia along an eco-
hyd ological g adien in a no he n aised bog complex.
En i on Mic obiol 7:1547–1557.
Juo onen H, Hynninen A, Nieminen M, Tuomi i a T, Tui ila
E-S, Nousiainen H, Kell DK, Y ja
¨la
¨K, Te ahau a A, F i ze H.
2012. Me hane-cycling mic obial communi ies and me hane
emission in na u al and es o ed pea lands. Appl En i on
Mic obiol 78:6386–6389.
Kaise C, F ank A, Wild B, Ko anda M, Rich e A. 2010. Negli-
gible con ibu ion om oo s o soil-bo ne phospholipid a y
acid ungal bioma ke s 18: 2x6, 9 and 18: 1x9. Soil Biol
Biochem 42:1650–1652.
Kip N, an Winden J, Pan Y, Bod ossy L, Reicha GJ, Smolde s
AJP, Je en MSM, Dams e
´JSS, Op den Camp HJM. 2010.
Global p e alence o me hane oxida ion by symbio ic bac e ia
in pea -moss ecosys ems. Na Geosci 3:617–621.
Ko hola A. 1992. Mi e induc ion, ecosys em dynamics and la -
e al ex ension on aised bogs in he sou he n coas al a ea o
Finland. Fenn-In J Geog 170:25–94.
Ko iaho M, F i ze H, Me ila
¨P, Tuomi i a T, Va
¨li an a M, Ko -
hola A, Ka o eld E, Tui ila ES. 2013. Ac inobac e ia com-
muni y s uc u e in he pea p o ile o bo eal bogs ollows a
a ia ion in he mic o opog aphical g adien simila o ege-
a ion. Plan Soil 369:103–114.
K oppens ed RM. 1985. Fa y acids and menaquinone analysis
o ac inomyce es and ela ed o ganisms. In: Good ellow M,
Minnikin DE, Eds. Chemical me hods in bac e ial sys ema ics,
. London: Academic P ess. pp 173–199.
Laiho R. 2006. Decomposi ion in pea lands: econciling seem-
ingly con as ing esul s on he impac s o lowe ed wa e le-
els. Soil Biol Biochem 38:2011–2024.
Laine AM, Meh a
¨ alo L, Tol anen A, F olking S, Tui ila E-S.
2019a. Combined e ec o d ainage, es o a ion and wa ming
on bo eal mi e g eenhouse gas luxes. Sci To al En i on
647:169–181.
Laine AM, Ma
¨ki an a P, Laiho R, Meh a
¨ alo L, Pen ila
¨T, Ko -
ensalo A, Minkkinen K, F i ze H, Tui ila E-S. 2019b.
Wa ming impac s on bo eal en CO
2
exchange unde we and
d y condi ions. Global Change Biol 25:1995–2008.
Laine AM, Lindholm T, Nilsson M, Ku zne so O, Jassey VEJ,
Tui ila ES. 2021. Func ional di e si y and ai composi ion o
ascula plan and Sphagnum moss communi ies du ing
pea land succession ac oss land upli egions. J Ecol
109:1774–1789.
Leppa
¨la
¨M, Kukko-Oja K, Laine J, Tui ila ES. 2008. Seasonal
dynamics o CO
2
exchange du ing p ima y succession o
bo eal mi es as con olled by phenology o plan s. Ecoscience
15:460–471.
Leppa
¨la
¨M, Laine AM, Se a
¨ki i ML, Tui ila ES. 2011a. Di e -
ences in CO
2
dynamics be ween successional mi e plan
communi ies du ing we and d y summe s. J Veg Sci 22:357–
366.
Leppa
¨la
¨M, Oksanen J, Tui ila ES. 2011b. Me hane lux
dynamics du ing mi e succession. Oecologia 165:489–499.
Lisboa FJG, Pe es-Ne o PR, Chae GM, Jesus EdC, Mi chell RJ,
Chapman SJ, Be be a RLL. 2014. Much beyond Man el:
b inging P oc us es associa ion me ic o he plan and soil
ecologis ’s oolbox. PLoS ONE 9:e101238.
Lu on PE, Wayne JM, Sha p RJ, Riley PW. 2002. The mc A gene
as an al e na i e o 16S RNA in he phylogene ic analysis o
me hanogen popula ions in land ill. Mic obiology 148:3521–
3530.
Ma
¨ki an a P, Laiho R, Meh a
¨ alo L, S ako a P, So munen J,
Minkkinen K, Pen ila
¨T, F i ze H, Tui ila E-S. 2018. Re-
sponses o phenology and biomass p oduc ion o bo eal ens o
clima e wa ming unde di e en wa e - able le el egimes.
Global Change Biol 24:944–956.
Med ede CA, B idgham SD, P ei e -Meis e L, Kelle JK. 2015.
Can Sphagnum leacha e chemis y explain di e ences in
anae obic decomposi ion in pea lands? Soil Biol Biochem
86:34–41.
Me ila
¨P, Galand PE, F i ze H, Tui ila ES, Kukko-oja K, Laine J,
Y ja
¨la
¨K. 2006. Me hanogen communi ies along a p ima y
succession ansec o mi e ecosys ems. FEMS Mic obiol Ecol
55:221–229.
Monie E, Sokolo A, Schlosse A, Sco J, Gao X. 2013. P ob-
abilis ic p ojec ions o 21s cen u y clima e change o e
No he n Eu asia. En i on Res Le 8:045008.
Oksanen J, Blanche FG, Kind R, Legend e P, Minchin PR,
OHa a RB, Simpson GL, Solymos P, Hen y M, S e ens H,
Wagne . 2015. egan: Communi y Ecology Package R package
e sion 2.3-0. h ps://CRAN.R-p ojec .o g/package= egan.
Pel oniemi K, F i ze H, Laiho R. 2009. Response o ungal and
ac inobac e ial communi ies o wa e -le el d awdown in
bo eal pea land si es. Soil Biol Biochem 41:1902–1914.
Pel oniemi K, S ako a
´P, F i ze H, Al i a I a
´izoz P, Pennanen T,
Laiho R. 2012. How wa e -le el d awdown modi ies li e -
decomposing ungal and ac inobac e ial communi ies in bo -
eal pea lands. Soil Biol Biochem 51:20–34.
Pel oniemi K, Laiho R, Juo onen H, Kiikkila
¨O, Ma
¨ki an a P,
Minkkinen K, Pennanen T, Pen ila
¨T, Sa jala T, Tui ila ES,
Tuomi i a TT, F i ze H. 2015. Mic obial ecology in a u u e
clima e: e ec s o empe a u e and mois u e on mic obial
communi ies o wo bo eal ens. FEMS Mic obiol Ecol
91: i 062.
Pel oniemi K, Laiho R, Juo onen H, Bod ossy L, Kell DK,
Minkkinen K, Ma
¨ki an a P, Meh a
¨ alo L, Siljanen HMP,
Tui ila ES, Tuomi i a TT, F i ze H. 2016. Responses o me-
hanogenic and me hano ophic communi ies o wa ming in
a ying mois u e egimes o wo bo eal ens. Soil Biol Bio-
chem 97:144–156.
Pennanen T, S o
¨mme R, Ma kkola A, F i ze H. 2001. Mic obial
and plan communi y s uc u e ac oss a p ima y succession
g adien . Scand J o Res 16:37–43.
Mic obes and C Fluxes in Pea land Succession
Pe es-Ne o PR, Jackson DA. 2001. How well do mul i a ia e da a
se s ma ch? The ad an ages o a P oc us ean supe imposi ion
app oach o e he Man el es . Oecologia 129:169–178.
Pe kioma
¨ki J, F i ze H. 2002. Sho and long- e m e ec s o
wood ash on he bo eal o es humus mic obial communi y.
Soil Biol Biochem 34:1343–1353.
Pu kinen A, La mola T, Tuomi i a T, Siljanen HMP, Bod ossy L,
Tui ila ES, F i ze H. 2014. Pea land succession induces a shi
in he communi y composi ion o Sphagnum-associa ed ac i e
me hano ophs. FEMS Mic obiol Ecol 88:596–611.
R Co e Team. 2014. R: a language and en i onmen o s a is ical
compu ing. Vienna: R Founda ion o S a is ical Compu ing.
Riu a T, Laine J, Tui ila ES. 2007. Sensi i i y o CO
2
exchange
o en ecosys em componen s o wa e le el a ia ion.
Ecosys ems 10:718–733.
Rob oek BJ, Jassey VE, Kox MA, Be endsen RL, Mills RT,
Ce
´cillon L, Puissan J, Meima-F anke M, Bakke PAHM,
Bodelie PL. 2015. Pea land ascula plan unc ional ypes
a ec me hane dynamics by al e ing mic obial communi y
s uc u e. J Ecol 103:925–934.
Rob oek BJ, Jassey VE, Bel man B, He ing MM. 2017. Di e se
en plan communi ies enhance ca bon- ela ed mul i unc-
ionali y, bu do no mi iga e nega i e e ec s o d ough . R
Soc Open Sci 4:170449.
Rosling A, Timling I, Taylo DL. 2013. A chaeo hizomyce es:
pa e ns o dis ibu ion and abundance in soil. In: Ho wi z B,
Mukhe jee P, Mukhe jee M, Kubicek C, Eds. Genomics o
soil-and plan -associa ed ungi, . Be lin: Sp inge . pp 333–349.
Roule N, Moo e T, Bubie J, La leu P. 1992. No he n ens:
me hane lux and clima ic change. Tellus B 44:100–105.
Smi h SE, Read DJ. 2008. Myco hizal symbiosis, 3 d edn.
Camb idge: Academic P ess. p 800.
So oco nola M, Laine A, Kiely G, By ne KA, Tui ila ES. 2009.
Vege a ion and en i onmen al a ia ion in an A lan ic blan-
ke bog in sou h-wes e n I eland. Plan Ecol 203:69–81.
S James AR, Ya i JB, Zinde SH, Richa dson RE. 2021. Linking
mic obial Sphagnum deg ada ion and ace a e mine aliza ion in
acidic pea bogs: om global insigh s o a genome-cen ic case
s udy. ISME J 15:293–303.
S ach JE, Maldonado LA, Wa d AC, Good ellow M, Bull AT.
2003. New p ime s o he class ac inobac e ia: applica ion o
ma ine and e es ial en i onmen s. En i on Mic obiol
5:828–841.
S ackeb and E. 2014. The amily Acidimic obiaceae. In: Rosen-
be g E, DeLong EF, Lo y S, S ackeb and E, Thompson F, Eds.
The p oka yo es, . Be lin: Sp inge . pp 5–12.
S ako a
´P, Pen ila
¨T, Laine J, Laiho R. 2012. Disen angling
di ec and indi ec e ec s o wa e able d awdown on abo e-
and belowg ound plan li e decomposi ion: consequences o
accumula ion o o ganic ma e in bo eal pea lands. Global
Change Biol 18:322–335.
S o
¨m L, Ekbe g A, Mas epano M, Ch is ensen TR. 2003. The
e ec o ascula plan s on ca bon u no e and me hane
emissions om a und a we land. Global Change Biol 9:1185–
1192.
Tah anainen T. 2011. Ab up omb o ophica ion o a bo eal
aapa mi e igge ed by hyd ological dis u bance in he
ca chmen . J Ecol 99:404–415.
Tsche ko D, Rus emeie J, Rich e A, Wanek W, Kandele E.
2003. Func ional di e si y o he soil mic o lo a in p ima y
succession ac oss wo glacie o elands in he Cen al Alps.
Eu J Soil Sci 54:685–696.
Tui ila ES, Juu inen S, F olking S, Va
¨li an a M, Laine AM,
Mie inen A, Me ila
¨P. 2013. We land ch onosequence as a
model o pea land de elopmen : Vege a ion succession, pea
and ca bon accumula ion. Holocene 23:25–35.
Tuomi i a TT, Y ja
¨la
¨K, F i ze H. 2009. Quan i a i e PCR o
pmoA using a no el e e se p ime co ela es wi h po en ial
me hane oxida ion in Finnish en. Res Mic obiol 160:751–
756.
U bano a
´Z, Ba
´ a J. 2016. E ec s o long- e m d ainage on
mic obial communi y composi ion a y be ween pea land
ypes. Soil Biol Biochem 92:16–26.
U bano a
´Z, Picek T, Ba
´ a J. 2011. E ec o pea e-we ing on
ca bon and nu ien luxes, g eenhouse gas p oduc ion and
di e si y o me hanogenic a chaeal communi y. Ecol Eng
37:1017–1026.
an B eemen N. 1995. How Sphagnum bogs down o he plan s.
T ends Ecol E olu 10:270–275.
Wel zin JF, Pas o J, Ha h C, B idgham SD, Updeg a K, Chapin
CT. 2000. Response o bog and en plan communi ies o
wa ming and wa e - able manipula ions. Ecology 81:3464–
3478.
Wood SN. 2006. Gene alized addi i e models: an in oduc ion
wi h R. Boca Ra on: Chapman and Hall/CRC.
Y ja
¨la
¨K, Tuomi i a T, Juo onen H, Pu kinen A, Lappi K,
Tui ila ES, Pen ila
¨T, Laine J, Pel oniemi K, F i ze H. 2011.
CH
4
p oduc ion and oxida ion p ocesses in a bo eal en
ecosys em a e long- e m wa e able d awdown. Global
Change Biol 17:1311–1320.
Yu ZC. 2012. No he n pea land ca bon s ocks and dynamics: a
e iew. Biogeosciences 9:4071–4085.
Zhou X, Zhang Z, Tian L, Xiujun Li, Tian C. 2017. Mic obial
communi ies in pea lands along a ch onosequence on he
Sanjiang Plain, China. Sci Rep 7:9567.
H. Juo onen and o he s