Photocatalyst-Free Visible Light-Induced Synthesis of β-Oxo Sulfones via Oxysulfonylation of Alkenes with Arylazo Sulfones and Dioxygen in Air

Article abstract of DOI:10.1002/adsc.201900984

A catalyst-free strategy has been established for the synthesis of β-oxo sulfones via visible light-induced oxysulfonylation of alkenes with arylazo sulfones with dioxygen in air. The present photoinduced transformation proceeds smoothly at room temperature in the absence of an external photosensitizer, which not only provides a mild and efficient approach to various β-oxo sulfones, but also opens a different reaction mode for the photochemical reaction of arylazo sulfones.

Full text of DOI:10.1002/adsc.201900984

PROF. HUI SUN (Orcid ID : 0000-0003-2015-6136)
Article type : Research Paper
The microbial diversity and structure in peatland forest in Indonesia
Bing Liua, Muhamed Jamal Hosen Talukdera, Eeva Terhonenb, Maija Lamplac, Harry
Vasanderc, Hui Suna*, Fred Asiegbuc*,
aCollaborative Innovation Center of Sustainable Forestry in Southern China, College of
Forestry, Nanjing Forestry University, Nanjing 210037, China
bDepartment of Forest Botany and Tree Physiology, Georg-August-Universität Göttingen,
Büsgenweg 2, 37077 Göttingen, Germany
cDepartment of Forest Sciences, University of Helsinki, Latokartanonkaari 7, P.O. Box 27,
00014, Helsinki, Finland
*Correspondence:
Hui Sun
College of Forestry, Nanjing Forestry University, Nanjing, China
No. 159, Longpan Road, 210037, Nanjing, China.
Tel: +8613851724350
e-mail: Hui.Sun@njfu.edu.cn
Fred Asiegbu
Department of Forest Sciences, University of Helsinki, Helsinki, Finland
Fred.asiegbu@helsinki.fi
This article has been accepted for publication and undergone full peer review but has not
been through the copyediting, typesetting, pagination and proofreading process, which may
lead to differences between this version and the Version of Record. Please cite this article as
doi: 10.1111/sum.12543
This article is protected by copyright. All rights reserved.

Running title:Microbial community in tropical peatland
Abstract
The microbial community structure and function under forest in tropical peatlands are poorly
understood. In this study, we investigated the microbial community structure and diversity in
natural peat swamp forest soil, disturbed peat soil and mineral soil in Central Kalimantan,
Indonesia, using 454 pyrosequencing. The results showed that the natural peat soil had the
greatest fungal species richness (Chao1), which was significantly (P < 0.05) larger than that
in the other two soils. Community structure of both fungi and bacteria in natural peat soil
differred significantly from that in the disturbed peat soil (P = 0.039 and P = 0.045,
respectively). Ascomycota (40.5%) was the most abundant phylum across the three soils
followed by Basidiomycota (18.8%), Zygomycota (< 0.1%) and Glomeromycota (< 0.1%).
The Linear discriminant analysis with Effect Size (LEfSe) showed that Ascomycota (P <
0.05) and genus Gliocephalotrichum (P < 0.05) dominated in natural peat soil. Functionally,
pathotrophs were more abundant in disturbed peat soil (P < 0.05). Proteobacteria (43.8%)
were the most abundant phylum followed by Acidobacteria (32.6%), Actinobacteria (9.8%),
Planctomycetes (1.7%). Methylocystis, Telmatospirillum, Syntrophobacter, Sorangium and
Opitutus were the more abundant genera in disturbed peat soil, whereas Nevskia and
Schlesneria were more abundant in mineral soil and natural peat soil, respectively. The
natural peat forest soil supported a more diverse microbiology, however, the land-use of such
a soil can change its microbial community structure. The results provide evidence that the
disturbance of tropical peat land could lead to the introduction and spread of a large number
of fungal diseases
This article is protected by copyright. All rights reserved.

Keywords: Tropical peatland, Microbes, Community structure, Diversity, 454
Pyrosequencing
1. Introduction
Tropical peat swamp forests in Southeast Asia are important ecosystems for conserving
unique biodiversity (Sorensen, 1993; Rieley et al., 2008; Harrison, 2013). Unfortunately, this
fragile ecosystem faces pressures from widespread anthropogenic impacts, e.g. deforestation,
drainage and fire, through agriculture, agroforestry and silviculture (Miettinen et al., 2017).
The change of peatlands from pristine forest to alternative uses is usually accompanied by
many negative effects on the environment including increased greenhouse gas emissions,
expanded carbon losses through aerobic peat decomposing, reduction of carbon sequestring
through photosynthesis and impacts on composition, diversity and function of soil
microorganisms community (Nakane et al., 1996; Oleszczuk et al., 2008; Artz, 2013; Puglisi
et al., 2014; Strickman et al., 2016).
Soil microorganisms play essential roles in peatland ecosystems via nutrient cycling and soil
organic matter (SOM) decomposition (Winsborough and Basiliko, 2010). Soil microbes are
instrumental in the control turnover of organic C in soil, which can in turn affect plant
photosynthesis and function of overall ecosystem (Andersen et al., 2013). Fungi represent a
key role in degradation of SOM in forest litter due to their ability to produce wide range of
hydrolytic and oxidative enzymes (Baldrian et al., 2013; Burns et al., 2013; Soudzilovskaia et
al., 2015). For example, white- and brown-rot fungi can degrade recalcitrant materials,
particularly for lignin, cellulose and hemicellulose (Floudas et al., 2012). In addition, many
ectomycorrhizal or ericoid mycorrhizal fungi can form symbiotic relationships with plants
(Sun et al., 2015). Relative to fungi, bacteria are the most abundant group of soil
This article is protected by copyright. All rights reserved.

microorganisms and are the first organisms to colonize dead wood and metabolize the easily
accessible substrates (Roesch et al., 2007; Schmidt et al., 2007). Bacteria may also produce
metabolites that functions as growth factors for fungi (Clausen 1996). Some bacteria may
equally compete for growth substrates with fungi and could be more active in aerobic
decomposition than fungal in peatland (Folman et al., 2010; Winsborough and Basiliko,
2010).
In recent years, many studies have focused on microbial communities in boreal peatland
based on culturing or PCR-based methods (Thormann et al., 2007; Peltoniemi et al., 2009;
Straková et al., 2011; Peltoniemi et al., 2012; Andersen et al., 2013; Zhao et al. 2017).
Differences in microbial communities between peatland types are driven by vegetation and
chemistry gradients, such as pH (Andersen et al., 2013). Fungi are more tolerant than bacteria
in low pH leading to fungal dominance in acid soils and bacterial diversity increased with
higher pH values (Högberg et al., 2007; Rousk et al., 2009; Shen et al., 2013; Liu et al.,
2014). However, compared to the boreal peatlands, the study of microbes under tropical
peatland forest is less common. One of these studies (Kanokratana et al., 2011) have reported
the bacterial diversity using pyrosequencing in forested peatlands in Thailand. Therefore, to
provide basic information on the microbial structure of tropical peat forest, we investigated
the microbial diversity and community structure in different tropical peat soils by 454
pyrosequencing technology. The aim of the study was to explore the impact of the use of
peatlands on the microbial communities in tropical peatlands.
This article is protected by copyright. All rights reserved.

2. Materials and methods
2.1 Study area and sampling
The study area was located in the province of Central Kalimantan in Indonesian Borneo
(2°19’ S, 113°54’ E). The average annual temperature varied between 25°C and 27°C and the
annual rainfall of the area was approximately 2700 mm, with the ‘wet’ season lasting from
November to April (Page et al., 2004). There were three sampling sites. The first site was in
a tropical peat swamp forest in the Sabangau National park in the Natural laboratory field
research area managed by CIMTROP (Center for International Cooperation in Sustainable
Management of Tropical Peatland). The highest ground surface elevation was 30 m a.s.l. This
location was almost pristine but with some signs of selective logging during 1970-1990.
Flooding occured frequently e.g. the water table stayed for six months within 31 cm range
(between −21 and +10 cm level), which in turn has affected the composition of the vegetation
community (Lampela et al., 2014). The vegetation consisted almost entirely of trees and tree
seedlings with very few other vascular plants or mosses. There have been more than 150 tree
species recorded in this peat swamp forest (Waldes & Page 2002) and the underlying peat
was formed of woody debris such as leaf litter, decaying roots, branches and fallen tree
trunks (Page et al. 1999; Lampela et al. 2014). Many of the trees formed buttress roots or
pneumatophores. Typical canopy tree species included Aglaia rubiginosa (Hiern Pannell),
Calophyllum hosei Ridl., C. lowii Hook.f., C. sclerophyllum Vesque, Combretocarpus
rotundatus (Miq.) Danser, Cratoxylum glaucum Korth., Dactylocladus stenostachys Oliv.,
Dipterocarpus coriaceus Slooten, Dyera costulata (Miq.) Hook.f., Ganua motleyana (de
Vriese) Pierre ex Dubard, Gonystylus bancanus (Miq.) Kurz, Neoscortechinia kingii (Hook.f.)
Pax & K.Hoffm., Palaquium cochlearifolium P.Royen, P. leiocarpum Boerl., Shorea
balangeran (Korth.) Burck, S. teysmanniana Dyer ex Brandis and Xylopia fusca Maingay ex
Hook.f. & Thomson (Page et al. 1999). The samples were taken from two nearby subregions
This article is protected by copyright. All rights reserved.

(S 2°19.376’, E 113°54.244’ and S 2°19.433’, E 113°54.268’) within the forest, 1.5 km away
from the forest edge. Three samples from the surface peat in each subregion were collected in
pristine peat forest.
The second and third sites were a disturbed peat soil and a mineral soil, respectively. The
disturbed site was in a degraded peat swamp area near the village Bereng Bengkel 15 km
southeast from Palangka Raya (S 2°13.481’, E 114°04.015’). The disturbed peat forest was a
burnt open area where the peat depth was 1 m and the vegetation consisted of only ferns
mainly including Polypodium sp. and Stenochlaena palustris. The area was drained and clear-
cut during Indonesian governmental land conversion and transmigration program “Mega Rice
Project” in 1996-97 and was used for low-intensity agriculture or was abandoned (Muhamad
& Rieley 2002; Page et al. 2002). The mineral forest soil was located in the canal edges not
far from the disturbed peat forest (S 2°13.659’, E 114°03.747’). The principal trees include
bananas (Musa sp.) and rubber trees (Hevea brasiliensis). The samples were collected in
September 2010. All the samples were taken into 50 ml sterile tubes after removing the soil
litter by hand using rubber gloves. The samples packed on ice and taken to the laboratory,
where they were kept at -20oC until subject to analysis. As there was a limited weight of
sample, soil physical and chemical properties at the three sites were not determined.
Characteristics of surface peat samples from two nearby subregions of natural peat swamp
forest were measured (Table S1).
2.2 DNA extraction and PCR amplification
Genomic DNA was extracted from 0.3 g of the homogenized soil per sample using the
PowerSoilTM DNA Isolation Kit according to the procedure recommended by the
manufacturer (MoBio Laboratories, Carlsbad, CA, USA). The DNA was quantified with a
Nanodrop-1000 spectrometer (NanoDrop Technologies, Wilmington, DE, USA). The Internal
This article is protected by copyright. All rights reserved.

Transcribed Spacer (ITS) region was amplified using the fungus-specific primers ITS1-F
(containing 454 pyrosequencing A adapter and a 6-bp barcode) and ITS4 (containing 454
pyrosequencing B adapter) (Gardes & Bruns, 1993; Terhonen et al., 2014). The cycling
reactions were performed using a PTC-100 Programmable Thermal Controller with the
following conditions: 94°C for 2 min; 30 cycles of 94°C for 30 s, 53°C for 1 min, and 72°C
for 1 min, followed by 10 min at 72°C. The bacterial primers 27 F (5'-Axxxxxx
AGAGTTTGATCCMTGGCTCAG-3') and 519R (5'-B GTATTACCGCGGCTGCTG-3')
were used to generate 16S rRNA gene fragments of ~ 500 bp from the variable regions V1-3.
The following thermal cycling scheme was used: 98°C for 30 s, 28 cycles of 10 s at 98°C,
59°C for 30 s and 72°C for 30 s, followed by 10 min at 72°C. The PCR amplicons were
determined and confirmed by analyzing 5 µl of product on 1.5% agarose gel. Amplicons
were cleaned by Agencourt AMPure XP beads (Beck-man Coulter) to remove amplification
primers and reaction buffer. After purification, DNA concentration was measured by Nano-
drop ND-1000 spectrophotometer and equivalent quantities (∼ 100 ng) of amplicons from
each sample were mixed in a single tube.
The PCR amplicons were sequenced using ITS1-F primer for fungi and 27 F primer for
bacteria at the Institute of Biotechnology (University of Helsinki Finland) using the 454 GS-
FLX titanium protocol (Life Science/Roche Diagnostics, CT, USA), which yielded read
lengths of 400 bp. The raw sequence data were submitted to Sequence Read Archive (SRA)
database (Accession Number: SRP172468 and 180939) in NCBI.
This article is protected by copyright. All rights reserved.

2.3 454 Pyrosequencing data processing
Sequence data were analyzed using the Mothur pipeline v. 1.39.2 with some modification
(Schloss et al., 2009). Briefly, the raw reads were exposed to quality control and each
sequence was separated for a match to the sequencing primer (ITS1-F or 27F) and valid DNA
tag. Sequences were discarded if they had (i) ambiguous (N) bases; (ii) homopolymers length
more than eight nucleotides; or (iii) an average Phred quality score lower than 25. Each
fungal sequences that passed the quality filtering was truncated to a 250-bp length. The
bacterial sequences were removed if the length was less than 400 bp or longer than 500 bp.
Due to the lack of fungal reference database for alignment, the fungal data were pairwise
aligned within the dataset. All potential chimeric sequences were categorized by using the
Mothur-embedded uchime de novo algorithm and discarded (Edgar et al., 2011). The high
quality and unique sequences were aligned by using the Needleman method (Needleman and
Wunsch, 1970) and then were clustered into operational taxonomic units (OTUs) using the
average neighbour joining algorithm 97% similarity. The whole sequence data set of fungi
was phylogenetically classified using a Mothur-formatted copy of the full UNITE+INSD data
sets version 6 with an 80% confidence threshold in Mothur. The sequences for bacterial
dataset were aligned to the SILVA alignment database and were clustered into OTUs defined
by a 97% similarity using the average neighbor algorithm (Yilmaz et al., 2007).
We also determined functional groups of fungal taxonomic affiliation by using FUNGuild
(Nguyen et al., 2016). The dataset could be divided into three trophic modes: pathotroph,
symbiotroph and saprotroph. Within these trophic modes, fungi were further divided into a
total of 12 categories.
This article is protected by copyright. All rights reserved.

Observed OTUs, species richness (Chao 1), diversity (Inverse Simpson’s complement),
species evenness (simpsonevenness) and Good’s coverage (complement of the ratio between
local singleton OTUs and the total sequence count) were calculated for both fungi and
bacteria in Mothur. The number of sequences of the lowest size (1,000 reads/sample for fungi
and 1886 for bacteria) among all samples was randomly subsampled (rarefaction) and used
for calculating the diversity index to ensure comparison between communities.
2.4 Statistical Analysis
Principle coordinate analysis (PCoA) was used to visualize the bacterial or fungal community
structure based on the relative abundance of OTUs in PRIMER 7+. Permutational
multivariate analysis of variance (PermANOVA) was used to test the difference in
community structure (Anderson, 2001). Mann-Whitney analysis was used to determine the
minimum significant difference (P < 0.05) in diversity index Chao1 and Simpson between
sites with SPSS 20.0 for Windows. Linear Discriminant Analysis (LDA) coupled with effect
size (LEfSe) was used to identify the fungal and bacterial taxa differentially represented
between sites (Segata et al., 2011). To hold as many taxa as possible for meaningful
comparisons and to remove all rare taxa in the analysis, we performed LEfSe by average
relative abundance of taxa > 0.0001.
3. Results
3.1 Information on pyrosequencing data
Due to the pyrosequence technical issue, two out of 12 samples were not sequenced properly.
The samples from the two plots in natural peat swamp were considerd as replicates for
natural peat swamp soil as the results showed that no differences were found for the two
plots. A total of 17 616 fungal ITS1 sequences and 22 187 bacterial 16S rDNA sequences
This article is protected by copyright. All rights reserved.

that passed quality control were obtained across the three sites. The number of fungal
sequences from each sample ranged from 1 022 to 2 142 with an average of 1 762 ± 360
(standard deviation). The number of bacterial sequences per sample ranged from 2 229 to 3
103 with an average of 2 466 ± 788 (standard deviation). A total of 1 000 sequences for
fungal data and 1 886 sequences for bacterial data were randomly subsampled from each
sample for comparative analysis among sites.
3.2 Overall fungal community diversity and composition
A total of 664 fungal operational taxonomic units (fOTUs) were estimated across the three
sites. The natural peat swamp soil had the greatest estimate of fOTU richness (Chao 1),
differing significantly from those from the other two sites (P < 0.05). The disturbed peat soil
had the least estimate of fOTUs (Table 1). No significant difference were found among the
three sites in fungal diversity (Inverse Simpson´s index 1/D) or Simpson evenness (Table 1).
All the fungal sequences were classified into four phyla. Ascomycota was the most abundant
phylum (40.5% of the total sequence) followed by Basidiomycota (18.8%), Zygomycota
(0.01%) and Glomeromycota (0.01%) (Figure 1). The most abundant orders were
Hypocreales (12.1%) and Polyporales (6.3%) (Figure 2). Some 11.1% of the fOTUs
representing 8.3% of the total sequences were further assigned to 45 genera or species levels.
The most abundant ones were ascomycete Williopsis (2.2%) (Figure 2).
3.3 Overall bacterial community diversity and composition
Altogether the bacterial sequences were divided into 1 408 bacterial OTUs (bOTU) across all
samples. No significant difference was observed for bOTU richness (Chao 1) among the three
sites (Table 1). However, the disturbed peat soil had the greatest bacterial diversity (Inverse
This article is protected by copyright. All rights reserved.

Simpson´s index 1/D) and Simpson evenness, being significantly greater than those in the
other two sites (P < 0.05) (Table 1).
Some 82.7% of the 1 408 bOTUs (90.2% of sequences) could be assigned to 11 phyla (Figure
3). Proteobacteria (37.6% of bOTUs) was the most abundant phylum followed by
Acidobacteria (21.2%), Actinobacteria (12.5%), Planctomycetes (6.0%), Verrucomicrobia
(1.5%) and TM7 group (1.1%). The sequences were further assigned into 45 genera and most
of them belonged to Acidobacteria (32.4% of sequences) and Proteobacteria (4.5% of
sequences). The most abundant genus in the three sites was Acidobacteria-Gp1 (28.8% of
sequences) followed by Acidobacteria-Gp2 (2.8% of sequences) and Burkholderia (1.7% of
sequences) (Figure 4).
3.4 Differences in the fungal communities among sites
The three sites only shared 2.1% of the 664 fOTUs and the percentage of unique fOTUs to
each site ranged from 12% to 53% accounting for 81.9% of the total fOTUs (Figure S1a).
The natural peat swamp soil had the highest number of unique fOTUs (352) and the disturbed
peat soil had the least number of unique fOTUs (80). The principal component analysis
(PCoA) based on the relative fOTUs abundance showed that the three sites formed distinct
community structure (Figure 5a). A total of 39.7% variation among the three sites was
observed and the first axis explained 21.8% of total variation and the second axis explained
17.9%. Subsequent Permanova analysis confirmed that the community structure in natural
peat swamp soil was significantly different from the mineral soil (P = 0.04) and the disturbed
peat soil (P = 0.039).
This article is protected by copyright. All rights reserved.

We investigated 201 fungi taxa at all levels to identify those differentially distributed
significantly between sites using LEfSe. At the phylum level, Ascomycota dominated in
natural peat swamp soil (Figure 6). At genus level, only Gliocephalotrichum appeared to be
enriched in natural peat swamp soil, whereas the mineral soil and the disturbed peat soil had
greater relative proportions of Penicillium and Gymnopilus, respectively (Figure 6).
For the functional groups, the saprotrophs were the most dominant fungal trophic guild across
all the sites followed by pathotrophs and symbiotrophs (Figure 7). The relative abundance of
pathotrophs in disturbed peat soil was significantly larger than in natural peat swamp soil or
mineral soil (P < 0.05) (Figure 7 and S2). In contrast, the abundance of dung saprotrophs and
wood saprotrophs in mineral soil was greater than in the two peat soils (P < 0.05). The
undefined saprotrophs in natural peat swamp soil were more abundant than in the other two
sites (P < 0.05).
3.5 Differences in the bacterial communities among sites
The three sites shared 15.1% of the 1408 bOTUs and the percentage of unique bOTUs at
each site ranged from 10.9% to 23.3% (Figure S1b). The natural peat swamp soil had the
most unique bOTUs, whereas mineral soil had the fewest unique bOTUs. The PCoA results
showed that the three sites formed distinct bacterial communities with 49.9% variation in
total and the community structure differed significantly between the natural peat swamp soil
and disturbed peat soil (P = 0.046) (Figure 5b).
In total, 259 bacterial taxa were included in LEfSe anlaysis. No significant differences in
abundance were observed at phylum level between sites. The taxa showing significant
differences between soils were presented in Figure 8. At genus level, the disturbed peat soil
This article is protected by copyright. All rights reserved.

had greater relative proportions of Methylocystis, Telmatospirillum, Syntrophobacter,
Sorangium and Opitutus, whereas only Nevskia was significantly more abundant in mineral
soil. The natural peat swamp soil had large relative proportions of Schlesneria and
Acidiphilium (Figure 8).
4. Discussion
In tropical peatland forest, the study of microbes is uncommon as previous research has maily
focused on the release of greenhouse gas from peatland combustion (Page et al., 2011;
Drösler et al., 2014; Bonn et al., 2016; Stockwell et al., 2016). Few studies have reported
how the land management practices in tropical peatland affect microbial diversity, using
cultivation, denaturing gradient gel electrophoresis, or restriction fragment length
polymorphism methods were used (Gilbert et al., 2008; Jackson et al., 2009; Kwon et al.,
2013). These methods may be insufficient to discern the effects of land use and management
on microbial communities as they can only analyze a limited group of microorganisms in
samples from complex tropical peatland environments. Therefore, in the current study, we
aimed to provide a more complete analysis of the fungal and bacterial communities in natural
and disturbed tropical peat soils as well as mineral soil by next-generation sequencing (454
pyrosequencing), which can collect information at higher quantitative resolutions and without
bias (Amend et al., 2010).
The α-diversity of fungi and bacteria were affected by disturbances in a different way. Fungal
richness (fOTUs) of natural peat swamp soil was significantly greater than that at the other
two sites, although fungal diversity was similar across the three sites. In contrast, bacterial
diversity in disturbed peat soil was significantly larger than at the other two sites. The smaller
bacterial diversity in natural peat swamp soil may be due to its considerably lower pH, as
This article is protected by copyright. All rights reserved.

previous studies observed that bacterial diversity increased with pH across a large range of
soil types ( Fierer & Jackson, 2006; Shen et al., 2013; Liu et al., 2014). Morover, other
studies have shown that fungi are more tolerant than bacteria to low pH, leading to fungal
dominance in acid soils (Högberg et al., 2007; Rousk et al., 2009). Consistent with this, we
showed that natural peat swamp soil the most fOTUs in our study. Similarly, fungal
saprotrophs are generally thought to play a more dominant role than bacteria in the upper
peatland layers, especially during the initial stages of litter decay (Williams and Crawford,
1983; Newell et al., 1995; Kuehn et al., 2000).
The fungal and bacterial community structures differed significantly among the three sites
with physico-chemical properties and landuse, consistent with previous studies (Kwon et al.,
2013; Hazard et al., 2014; Mishra et al., 2014; Ciccolini et al., 2016). In pristine peatland,
photosynthesis leads to carbon inputs which exceed the losses caused by decomposition,
resulting in net accumulation (Slater et al., 2009; Andersen et al., 2013). Nevertheless, the
fungi and bacteria in pristine peatlands have developed physiological and metabolic
adaptations to cope with the constraints in these ecosystems, such as low oxygen availability,
acidity or oligotrophy (Andersen et al., 2013). However, previous studies have shown that
different microbial groups in the community respond differently to changes in plant and soil
characteristics caused by changes in land properties and use (Andersen et al., 2013; Kwon et
al., 2013; Hazard et al., 2014; Mishra et al., 2014; Ciccolini et al., 2016). In our study,
microbial populations were sensitive to changes in pH, groundwater table, plant community
composition and litter quality caused by land clearance and drainage. Generally, fungi play a
fundamental role in the decomposition of organic matter in many acidic terrestrial ecosystems
because of their low demand for nitrogen and other nutrients and ability to transport nutrients
through the hyphal networks (Williams & Crawford 1983; Thormann et al., 2002; Andersen
This article is protected by copyright. All rights reserved.

et al., 2013). In contrast, one of the major restraints on the composition of bacterial
communities is that they need to extract energy for pumping hydrogen ions out of cells in
order to survive in acidic and oligotrophic conditions (Dedysh et al.,1998; Fierer & Jackson,
2006).
Microbial taxonomic composition varied greatly between the three sites. In natural peat
swamp soil, Ascomycota accounted for nearly half of the total sequences and dominated the
fungal community, which is consistent with the previous results obtained from boreal
peatland soil (Peltoniemi et al., 2009; Sun et al., 2016). Basidiomycota, the second dominant
phylum in the natural peat swamp soil, did not differ in abundance among the three sites.
Polyporales, which are special wood-degrading fungi and belonging to Agaricomycetes,
accounted for 6.3% of the fungi sequences across all sites and was a positively discriminant
taxon for natural peat swamp soil. The white-rot genera Ganoderma, Phlebia and
Perenniporia of Polyporales had greater abundance as well in the studied sites. The above
genera have the unique ability to decay lignin (Capelari & Zadrazil, 1997; Baldrian et al.,
2003; Ben et al., 2007; Isroi et al., 2011), which was also supported by the functional
analysis in our study. Surprisingly, the results are not in line with the observation obtained
from boreal peat soil, in which certain white and brown fungi are common, but with low
abundance (Thormann and Rice, 2007; Ovaskainen et al., 2013; Sun et al., 2016). The large
amplitude of water level and high temperature in tropical peatland (Jauhiainen et al., 2014)
might contribute to the abundance of Polyporales species in our study. In natural peatland, the
plants of dipterocarp forming association with Ectomycorrhiza (ECM), e.g. D. coriaceus and
S. balangeran are more dominant (Sirikantaramas et al., 2003), which might contribute to the
abundance of Thelephoraceae. In contrast, members of the order Sebacinales and the genus
Gymnopilus belonging to Agaricales were enriched in disturbed peat soil. Generally,
This article is protected by copyright. All rights reserved.

Sebacinales and Agaricales (e.g., Gymnopilus and Psathyrella) belonging to Agaricomycetes
play an important role in the decomposition of organic matter such as lignin or cellulose in
tropical zones (Capelari & Zadrazil, 1997). Our finding confirmed that drought may
accelerate degradation of the most complex organic matter such as lignocellulose of peats
(Davidson and Janssens, 2006; Fenner and Freeman, 2011). Furthermore, fewer plant species
and aerobic conditions, which are beneficial to the competition of some bacteria, can result in
the decrease of fungal richness (Gilbert et al., 2008; Folman et al., 2010; Winsborough and
Basiliko, 2010). In functional traits, the pathotrophic fungi were over-represented in disturbed
peat soil due to the presence of species of Metarhizium and Pestalotiopsis, which cause
tropical plant disease (Putten et al., 1993; Ansari et al., 2007; Sepiah and Lit, 2004). This
suggests that the disturbance of tropical peat land might lead to the introduction and spread of
a large number of fungal diseases (Putten et al., 1993; Gilbert & Morgan 2013; Murphy, 2014).
Moreover, the saprotrophic fungal orders Eurotiales and Trichosphaeriales were more
abundant in mineral soils, which is in agreement with the previous work that the filamentous
hyphae growth of some degrading fungi are unrestricted in mineral soils and in rich organic
matter soil (Thormann et al., 2001; Thormann et al., 2002; Andersen et al., 2013). For
example, Sordariomycetes, such as Trichosphaeriales, had greater abundance in soil rich in
organic matter and plant residues ( Zhao et al., 2017). Based on current databases, a larger
percentage of fungal sequences (nearly 60% of the sequences) could not be classified into any
fungal phyla. This indicates that many fungi in tropical peat soils and mineral soils are still
unknown and require further investigation.
Symbiotrophic fungi were not abundant and there was no difference among the three sites.
Previous studies have demonstrated that saprotrophic fungi are more abundant in the litter
horizon of the forest floor, whereas symbiotrophic fungi increase in abundance with depth of
This article is protected by copyright. All rights reserved.

soil in boreal forest (Lindahl et al., 2007). One possible explanation is that peat soils have
unique rapid degradation ability with large spatial heterogeneity of fungal communities in
different regions of the soil (Kelly et al., 2014; Sun et al., 2016). Alternatively, it might be
due to the community change from a mycorrhizal dominant to a saprotrophic dominant
community with increasing decomposition stage in peatland (Peltoniemi et al., 2012). The
abundance of Russula spp. was negatively correlated with the abundance of other
ectomycorhizal fungi (Koide et al., 2005). The distribution and difference in mycorrhizal
functional groups may be dependent on the restriction of limiting sampling to top soil.
Therefore, it is necessary to further study the function and diversity of the mycorrhizal
community with deeper samples from tropical peat soils.
Proteobacteria and Acidobacteria were the most abundant phyla across all the samples. The
two phyla have been reported as dominant groups in natural tropical peat swamp forest in
Southern Thailand and native Atlantic Rain Forest (peatland) in Southern Brazil
(Kanokratana et al., 2011; Etto et al., 2014). Soil bacteria community structure is related to
local environmental problems, especially with soil acidity in the tropical region, such as those
of the current study (Zhang et al., 2016). Proteobacteria and Acidobacteria can indicate signs
of nutrient status due to differences in their metabolism (Hartman et al., 2008). A soil with
more organic carbon is associated to a high abundance of Proteobacteria, while oligotrophic
conditions favor Acidobacteria (Lin et al., 2011). Moreover, the abundance of the
Acidobacteria is associated to acidic environment (Philippot et al., 2010). The Alpha-
proteobacteria and Acidobacteria-Gp1 were the dominant class in all sites. Many genera of
Acidobacteria (Gp1, 2, 3, 4, 5 and 13) were currently detected compared to previous study, in
which only Gp1, 2 and 3 were more common (Bunterngsook et al., 2010). This indicates a
high diversity of Acidobateria in this acidic tropical peatland ecosystems. The environment of
This article is protected by copyright. All rights reserved.

poor nutrient and low pH humid wetland forests is thought to favor Acidobacteria (Gp1, 2,
and 3) (Jamas, 2011; Bartram et al., 2014). However, of all bacterial taxa, only Schlesneria
and Acidiphilium were significantly more abundant in natural peat swamp soil. This finding
confirmed that low pH and nutrient conditions in peat soil limit the diversity and composition
of bacterial communities (Dedysh et al.,1998; Fierer & Jackson, 2006). Conversely, 11
bacterial taxa, such as Methylocystis, Telmatospirillum, Syntrophobacter, Sorangium and
Opitutus, were more abundant in disturbed peat soil. Fore instance, Sorangium is a genus of
Myxobacteria, which degrades cellulose and produces secondary metabolites to inhibit fungi
(Ringel, 1978). Previous studies have also shown that the diversity and richness of fungi are
reduced by the fact that some bacteria may compete with fungi of organic matter (Folman et
al., 2010; Winsborough and Basiliko, 2010). The other four genera are also involved in the
carbon degradation of peatland and interact with each other in CH4 metabolic pathway. For
instance, members of Opitutus are capable of degrading cellulose to propionate, a
methanogenic precursor (Chin & Janssen, 2002). Some species of Syntrophobacter, such as S.
fumaroxidans, can interact with methanogens to oxidize propionate through formic acid as an
electron carrier (Stams et al., 2002; Muller et al., 2010). Methylocystis, can synthesizes
methane monooxygenase (MMO) enzyme, which enables it to metabolize CH4 to produce
biomass and CO2 (Hanson & Hanson, 1996; Mcdonald et al., 2008). The abundance of
Methylocystis can reflect the decrease of water level and the increase of pH in disturbed peat
soil than in natural peat swamp soil (Dunfield et al., 1993; Gulledge & Schimel 1998). The
latest study of the high-quality draft genome sequence of Telmatospirillum siberiense in
Siberian peatland reveals the expected and novel metabolic potential for sulfur oxidation of
the genus Telmatospirillum (Hausmann et al., 2018). Therefore, how Telmatospirillum affect
CH4 metabolism by participating in sulfur cycle remains to be further studied. Similarly, due
to the absence of archaeal data, methanogens, which is an important groups in methane
This article is protected by copyright. All rights reserved.

metabolism, need to be further studied. In mineral soil, the most abundant bacteria taxa were
Firmicutes (class Bacilli and its order Bacillales) and Proteobacteria (order Caulobacterales,
its family Caulobacteraceae, family Sinobacteraceae and its genus Nevskia). The phylum
Firmicutes is known for species that synthesize high levels of secondary metabolites (Kim et
al., 2011; Palaniyandi et al., 2013). However, the soil properties were not measured due to
the limited volumn of samples in our study. Therefore, further studies are necessary to
investigate the microbial functions and the relationships between microbial community and
environmental factors.
Our result also revealed that current land use and management in peatland areas, such as
drainage and land clearing, have a negative impact on the microbial community. The many
human induced land use changes observed in the tropical peatlands all cause groundwater
levels to be lowered and plant and soil properties to be changed as a result of drainage and
land clearing (Henk et al., 2006; Andersen et al., 2013). The lowering of the groundwater
level in the tropical ecosystem are likely to change the microbial community in this
ecosystem thus, accelerating the degradation of materials such as lignocellulose of peats
(Davidson & Janssens, 2006; Jaatinen et al., 2007; Jaatinen et al., 2008; Fenner & Freeman,
2011). One outcome of this occurrence of events is increased CO2 and CH4 emission. An
innovative alternative practice to stabilize the peat soils is using an admixture to minimize
microbial decomposition of peatlands and emissions of greenhouse gas (Wong et al., 2009;
Canakci et al., 2015). However, the health of peat properties and soil microorganisms could
be negatively affected by binder method (Leng et al., 2019). The high temperature and the
lowering of the groundwater level in the tropical peatlands also increase the risk of fire
because of dominant cellulose, hemicellulose and lignin compounds in the peat (Usup et al.,
2004). Therefore, the optimum restoration and conservation planning for peatland should
This article is protected by copyright. All rights reserved.

include the restoration of water level and native plant community (Henk et al., 2006; Leng et
al., 2019).
5. Conclusion
This study provided new insight for understanding the impact of different land management
practices on microbial community structures in tropical peat forest soil - a unique ecosystem.
The natural peat forest harbored more diverse microbes, in which Ascomycota and
Proteobacteria were the most abundant fungal and bacterial phylum, respectively. The
pathotrophs were more abundant in disturbed peat soil suggesting the disturbance of natural
peat forest can lead to changes in microbial community diversity and structure as well as
more potential plant diseases.
Acknowledgements
The Academy of Finland is gratefully acknowledged for research funding. The research
funding for Jiangsu Specially-Appointed Professor (project 165010015), Priority Academic
Program Development of Jiangsu Higher Education Institutions (PAPD) and The National
Natural Science Fund of China (31870474) are also acknowledged. The authors wish to
acknowledge CSC – IT Center for Science, Finland, for generous computational resources.
This article is protected by copyright. All rights reserved.

References
Amend AS, Seifert KA, Bruns TD. 2010. Quantifying microbial communities with 454
pyrosequencing: does read abundance count? Mol Ecol 19: 5555–5565.
Anderson M J. 2001. A new method for non- parametric multivariate analysis of variance. Austral
Ecology, 26, 32–46.
Andersen R, Chapman S J, Artz R R E. 2013. Microbial communities in natural and disturbed
peatlands: A review[J]. Soil Biology & Biochemistry, 57(3):979-994.
Ansari M A, Shah F A, Whittaker M, et al. 2007. Control of western flower thrips (Frankliniella
occidentalis) pupae with Metarhizium anisopliae in peat and peat alternative growing media[J].
Biological Control, 40(3):293-297.
Artz, R. R. E. . 2013. Microbial Community Structure and Carbon Substrate use in Northern
Peatlands. Carbon Cycling in Northern Peatlands. American Geophysical Union.
Baldrian P. 2003. Interactions of heavy metals with white-rot fungi[J]. Enzyme & Microbial
Technology, 32(1):78-91.
Baldrian, Petr, Vetrovsky, et al. 2013. Estimation of fungal biomass in forest litter and soil[J]. Fungal
Ecology, 6(1):1-11.
Bartram, A. K. , Jiang, X. , Lynch, M. D. J. , Masella, A. P. , Nicol, G. W. , & Dushoff, J. , et al. 2014.
Exploring links between ph and bacterial community composition in soils from the craibstone
experimental farm. Fems Microbiology Ecology,87(2).
Ben Y S, Mechichi T, Sayadi S. 2007. Purification and characterization of the laccase secreted by the
white rot fungus Perenniporia tephropora and its role in the decolourization of synthetic dyes.[J].
Journal of Applied Microbiology, 102(4):1033-1042.
Bonn, A. , Allott, T. , Evans, M. , Joosten, H. , & Stoneman, R. . (2016). Peatland restoration and
ecosystem services (science, policy and practice): ecosystem services, degradation and restoration of
peat swamps in the south east asian tropics. ,10.1017/CBO9781139177788(14), 253-288.
This article is protected by copyright. All rights reserved.

Bunterngsook B, Kanokratana P, Thongaram T, et al. 2010. Identification and Characterization of
Lipolytic Enzymes from a Peat-Swamp Forest Soil Metagenome[J]. Journal of the Agricultural
Chemical Society of Japan, 74(9):1848-1854.
Burns R G, Deforest J L, Marxsen J, et al. 2013. Soil enzymes in a changing environment: Current
knowledge and future directions[J]. Soil Biology & Biochemistry, 58(2):216-234.
Canakci, H., Sidik, W., & Kilic, I. H. 2015. Bacterail calcium carbonate precipitation in peat. Arabian
Journal for Science & Engineering, 40(8), 2251-2260.
Capelari, M. , & Zadrazil, F. . 1997. Lignin degradation andin vitrodigestibility of wheat straw treated
with brazilian tropical species of white rot fungi. Folia Microbiologica, 42(5), 481-487.
Chin, K. J. , & Janssen, P. H. . 2002. Propionate formation by opitutus terrae in pure culture and in
mixed culture with a hydrogenotrophic methanogen and implications for carbon fluxes in anoxic rice
paddy soil. Applied and Environmental Microbiology, 68(4), 2089-2092.
Ciccolini, V. , Ercoli, L. , Davison, J. , Vasar, M. , öpik, Maarja, & Pellegrino, E. . 2016. Land-use
intensity and host plant simultaneously shape the composition of arbuscular mycorrhizal fungal
communities in a mediterranean drained peatland. FEMS Microbiology Ecology, fiw186.
Clausen C A. 1996. Bacterial associations with decaying wood: a review[J]. International
Biodeterioration & Biodegradation, 37(1–2):101-107.
Davidson, E. A. , & Janssens, I. A. . 2006. Temperature sensitivity of soil carbon decomposition and
feedbacks to climate change. Nature, 440(7081), 165-173.
Dedysh, S. N. , Panikov, N. S. , & Tiedje, J. M. . 1998. Acidophilic methanotrophic communities
from Sphagnum peat bogs. Applied & Environmental Microbiology, 64(3), 922.
Drösler M, Verchot L V., Freibauer A et al. 2014. Chapter 2: Drained inland organic soils. In: 2013
Supplement to the 2006 IPCC Guidelines for National Greenhouse Gas Inventories: Wetlands (eds
Hiraishi T, Krug T, Tanabe K, Srivastava N, Jamsranjav B, Fukuda M, Troxler T), pp. 1–79. IPCC,
Switzerland.
This article is protected by copyright. All rights reserved.

Dunfield P., Knowles R., and Dumont R., 1993, Methane production and consumption in temperate
and subarctic peat soils:response to temperature and pH, Soil Biology and Biochemistry, 25(3): 321-
326
Edgar R C, Haas B J, Clemente J C, et al. 2011. UCHIME improves sensitivity and speed of chimera
detection[J]. Bioinformatics, 27(16):2194.
Etto, R. M., Cruz, L. M., Da, C. J. E., et al. 2014. Seasonal changes in dominant bacterial taxa from
acidic peatlands of the atlantic rain forest. Research in Microbiology, 165(7), 517-525.
Fenner, N., & Freeman, C. 2011. Drought-induced carbon loss in peatlands. Nature Geoscience, 4(12),
895-900.
Ferris H & Tuomisto H. 2015. Unearthing the role of biological diversity in soil health[J]. Soil
Biology and Biochemistry, 85, 101-109.
Fierer, N., & Jackson, R. B. 2006. The diversity and biogeography of soil bacterial
communities. Proceedings of the National Academy of Sciences of the United States of
America, 103(3), 626-631.
Floudas D, Binder M, Riley R, et al. 2012. The Paleozoic origin of enzymatic lignin decomposition
reconstructed from 31 fungal genomes.[J]. Science, 336(6089):1715-1719.
Folman L B, Gunnewiek P J A K, Boddy L, et al. 2010. Impact of white-rot fungi on numbers and
community composition of bacteria colonizing beech wood from forest soil[J]. Fems Microbiology
Ecology, 63(2):181-191.
Gardes, M. , & Bruns, T. D. . 1993. Its primers with enhanced specificity for basidiomycetes -
application to the identification of mycorrhizae and rusts. Molecular Ecology Notes, 2, 113-118.
Gilbert, G. S. , Gorospe, J. , & Ryvarden, L. . 2008. Host and habitat preferences of polypore fungi in
micronesian tropical flooded forests. Mycological Research, 112(6), 674-680.
Gilbert, L. , & Morgan, E. . 2013. Can restoration of afforested peatland regulate pests and
disease?. Journal of Applied Ecology, 50(5), n/a-n/a.
This article is protected by copyright. All rights reserved.

Gulledge, J. , & Schimel, J. P. . 1998. Moisture control over atmospheric CH4 consumption and CO2
production in diverse alaskan soils. Soil Biology & Biochemistry, 30(8–9), 1127-1132.
Hausmann, B. , Pjevac, P. , Schreck, K. , Herbold, C. W. , Daims, H. , & Wagner, M. , et al. 2018.
Draft genome sequence of Telmatospirillum siberiense, 26-4b1, an acidotolerant peatland
alphaproteobacterium potentially involved in sulfur cycling. Genome Announcements, 6(4), e01524-
17.
Hanson, R. S., & Hanson, T. E. 1996. Methanotrophic bacteria. Microbiological Reviews, 60(2), 439-
71.
Harrison, M. E. 2013. Using Conceptual Models to Understand Ecosystem Function and Impacts of
Human Activities in Tropical Peat-swamp Forests. Wetlands, 33, 257-267.
Hartman W H, Ricardson C J, Vilgalys R & Bruland G L. 2008. Environmental and anthropogenic
controls over bacterial communities in wetland soils. Proceedings of the National Academy of
Sciences, 105, 17842-17847.
Hazard, C. , Gosling, P. , Mitchell, D. T. , Doohan, F. M. , & Bending, G. D. . 2014. Diversity of
fungi associated with hair roots of ericaceous plants is affected by land use. FEMS Microbiology
Ecology, 87(3), 586-600.
Henk W, Aljosja H, Christian, Dipa S. R., Aswandi I. & John R. 2006. Tropical peatland water
management modelling of the air hitam laut catchment in indonesia. International Journal of River
Basin Management, 4(4), 233-244.
Högberg, M. N. , Hogberg, P. , & Myrold, D. D. . 2007. Is microbial community composition in
boreal forest soils determined by ph, c-to-n ratio, the trees, or all three?. Oecologia (Berlin), 150(4),
590-601.
Isroi I, Millati R, Niklasson C, et al. 2011. Biological treatment of Lignocelluloses with white-rot
funghi and its applications: Review[J]. Bioresources, 6(4):5224-5259.
Jaatinen, K. , Fritze, H. , Laine, J. , & Laiho, R. . 2007. Effects of short- and long-term water-level
This article is protected by copyright. All rights reserved.

drawdown on the populations and activity of aerobic decomposers in a boreal peatland. Global
Change Biology, 13(2), 491-510.
Jaatinen, K. , Laiho, R. , Vuorenmaa, A. , Castillo, U. D. , & Fritze, H. . 2008. Responses of aerobic
microbial communities and soil respiration to water-level drawdown in a northern boreal
fen. Environmental Microbiology, 10(2), 339-353.
Jackson, C. R. , Liew, K. C. , & Yule, C. M. . 2009. Structural and functional changes with depth in
microbial communities in a tropical malaysian peat swamp forest. Microbial Ecology, 57(3), 402-412.
James J Hoorman. 2011. The role of soil bacteria, fact sheet agriculture and natural resources, Ohio
State University.
Jauhiainen, J. , Kerojoki, O. , Silvennoinen, H. , Limin, S. , & Vasander, H. . 2014. Heterotrophic
respiration in drained tropical peat is greatly affected by temperature—a passive ecosystem cooling
experiment. Environmental Research Letters, 9(10), 105013.
Kanokratana, P. , Uengwetwanit, T. , Rattanachomsri, U. , Bunterngsook, B. , Nimchua, T. , &
Tangphatsornruang, S. , et al. 2011. Insights into the phylogeny and metabolic potential of a primary
tropical peat swamp forest microbial community by metagenomic analysis. Microbial Ecology, 61(3),
518-528.
Kelly, T. J. , Baird, A. J. , Roucoux, K. H. , Baker, T. R. , EurÃdice N. Honorio Coronado, & Marcos
RÃos, et al. 2014. The high hydraulic conductivity of three wooded tropical peat swamps in northeast
peru: measurements and implications for hydrological function. Hydrological Processes, 28(9), 3373-
3387.
Kim, Y. C. , Leveau, J. , Mcspadden Gardener, B. B. , Pierson, E. A. , Pierson, L. S. , & Ryu, C. M. .
2011. The multifactorial basis for plant health promotion by plant-associated bacteria. Applied and
Environmental Microbiology, 77(5), 1548-1555.
Koide R T, Xu B, Sharda J, et al. 2005. Evidence of species interactions within an ectomycorrhizal
fungal community.[J]. New Phytologist, 165(1):305.
This article is protected by copyright. All rights reserved.

Kwon, M. J. , Haraguchi, A. , & Kang, H. . 2013. Long-term water regime differentiates changes in
decomposition and microbial properties in tropical peat soils exposed to the short-term drought. Soil
Biology and Biochemistry, 60, 33-44.
Kuehn, K. A. , Lemke, M. J. , & Wetzel, K. S. G. . (2000). Microbial biomass and production
associated with decaying leaf litter of the emergent macrophyte juncus effusus. Limnology and
Oceanography, 45(4), 862-870.
Lampela M, Jauhiainen J, Vasander H. 2014. Surface peat structure and chemistry in a tropical peat
swamp forest[J]. Plant & Soil, 382(1-2):329-347.
Leng, L. Y. , Ahmed, O. H. , & Jalloh, M. B. . 2019. Brief review on climate change and tropical
peatlands. Geoscience Frontiers, S1674987118300343.
Lin, X. , Tfaily, M. M. , Steinweg, J. M. , Chanton, P. , Esson, K. , & Yang, Z. K. , et al. 2014.
Microbial community stratification linked to utilization of carbohydrates and phosphorus limitation in
a boreal peatland at marcell experimental forest, minnesota, usa. Applied and Environmental
Microbiology,80(11), 3518-3530.
Lin Y T, Kamlesh J, Williamb W, et al. 2011. Soil bacterial communities in native and regenerated
perhumid montane forests[J]. Applied Soil Ecology, 47(2):111-118.
Lindahl B D, Ihrmark K, Boberg J, et al. 2007. Spatial separation of litter decomposition and
mycorrhizal nitrogen uptake in a boreal forest.[J]. New Phytologist, 173(3):611-620.
Liu, J. , Sui, Y. , Yu, Z. , Shi, Y. , Chu, H. , & Jin, J. , et al. 2014. High throughput sequencing
analysis of biogeographical distribution of bacterial communities in the black soils of northeast
china. Soil Biology and Biochemistry, 70, 113-122.
Mcdonald, I. R., Bodrossy, L., Chen, Y., & Murrell, J. C. 2008. Molecular ecology techniques for the
study of aerobic methanotrophs. Applied & Environmental Microbiology, 74(5), 1305-15.
Miettinen, J., Hooijer, A., Vernimmen, R., Liew, S.C., Page, S.E., 2017. From carbon sink to carbon
source: extensive peat oxidation in insular Southeast Asia since 1990. Environmental Research
This article is protected by copyright. All rights reserved.

Letters 12(2), 024014
Mishra S, Lee W. A., Hooijer A., Reuben S., Sudiana I. M., Idris A., and Swarup S. 2014. Microbial
and metabolic profiling reveal strong influence of water table and land-use patterns on classification
of degraded tropical peatlands. Biogeosciences, 11, 1727–1741.
Mueller, R. C. , Paula, F. S. , Mirza, B. S. , Rodrigues, J. L. , & Bohannan, B. J. . 2014. Links
between plant and fungal communities across a deforestation chronosequence in the amazon
rainforest. The ISME Journal, 8(7).
Muhamad NZ, Rieley JO. 2002. Management of tropical peatlands in Indonesia: mega reclamation
project in Central Kalimantan. In Peatlands for People, Natural Resources Function and Sustainable
Management, Rieley JO, Page SE (eds). with Setiadi B. Proceedings of the International Symposium
on Tropical Peatland, 22–23 August 2001, Jakarta, Indonesia. BPPT and Indonesian Peat Association:
Jakarta;155–160.
Murphy D. P., 2014. The future of oil palm as a major global crop: opportunities and challenges. J.
Oil Palm Res.Vol. 26(1): 1-24.
Nakane K, Ohno T Horikoshi T. 1996. Root respiration rate before and just after clear-felling in a
mature, deciduous, broad-leaved forest. Ecological Research, 11(2), 111-119.
Needleman S B, Wunsch C D. 1970. A general method applicable to the search for similarities in the
amino acid sequence of two proteins ☆[J]. Journal of Molecular Biology, 48(3):443-453.
Newell, S. Y. , Moran, M. A. , Wicks, R. , & Hodson, R. E. . (1995). Productivities of microbial
decomposers during early stages of decomposition of leaves of a freshwater sedge. Freshwater
Biology, 34(1), 135-148.
Nguyen N H, Song Z, Bates S T, et al. 2016. FUNGuild: An open annotation tool for parsing fungal
community datasets by ecological guild[J]. Fungal Ecology, 20(1):241-248.
Oleszczuk R, Regina K, Szajdak L, and Hoper H & Maryganova V. 2008. Impacts of agricultural
utilization of peat soils on the greenhouse gas balance. In: STRACK, M. (ed.) Peatlands and climate
This article is protected by copyright. All rights reserved.

change. Jyvaskyla, Finland: International Peat Society.
Ovaskainen O, Schigel D, Alikovero H, et al. 2013. Combining high-throughput sequencing with fruit
body surveys reveals contrasting life-history strategies in fungi[J]. Isme Journal, 7(9):1696.
Page, S. E. , Rieley, J. O. , Shotyk, O. W. , & Weiss, D. . 1999. Interdependence of peat and
vegetation in a tropical peat swamp forest. Philosophical Transactions B, 354(1391), 1885-1897.
Page, S. E. , Siegert, F. , Rieley, J. O. , Boehm, H. D. V. , Jaya, A. , & Limin, S. . 2002. The amount
of carbon released from peat and forest fires in indonesia during 1997. Nature (London), 420(6911),
61-65.
Page, S. E. , R. A. J. Wűst, Weiss, D. , Rieley, J. O. , Shotyk, W. , & Limin, S. H. . 2004. A record of
late pleistocene and holocene carbon accumulation and climate change from an equatorial peat bog
(kalimantan, indonesia): implications for past, present and future carbon dynamics. Journal of
Quaternary Science, 19(7), 625-635.
Page, S. E., Rieley, J. O., & Banks, C. J. 2011. Global and regional importance of the tropical
peatland carbon pool. Global Change Biology,17(2), 798-818.
Palaniyandi, S. A. , Yang, S. H. , Zhang, L. , & Suh, J. W. . 2013. Effects of actinobacteria on plant
disease suppression and growth promotion. Applied Microbiology and Biotechnology,97(22), 9621-
9636.
Pankratov, T. A. , Belova, S. E. , & Dedysh, S. N. . 2006. Evaluation of the phylogenetic diversity of
prokaryotic microorganisms insphagnumpeat bogs by means of fluorescence in situ hybridization
(fish). Microbiology, 74(6), 722-728.
Peltoniemi, K. , Fritze, H. , & Laiho, R. . 2009. Response of fungal and actinobacterial communities
to water-level drawdown in boreal peatland sites. Soil Biology & Biochemistry, 41(9), 1902-1914.
Peltoniemi, K. , Petra Straková, Fritze, H. , Pablo Alvira Iráizoz, Pennanen, T. , & Laiho, R. . 2012.
How water-level drawdown modifies litter-decomposing fungal and actinobacterial communities in
boreal peatlands. Soil Biology & Biochemistry, 51(2012), 20-34.
This article is protected by copyright. All rights reserved.

Philiport L, Andersson S G E, Battin TJ, Whitman WB, Hallin S. 2010. The ecological coherence of
high bacterial taxonomic ranks, Nat.Rev. Microbial.8, 523-529.
Puglisi E, Zaccone C, Cappa F, et al. 2014. Changes in bacterial and archaeal community
assemblages along an ombrotrophic peat bog profile[J]. Biology & Fertility of Soils, 50(5):815-826.
Putten, W. H. V. D. , Dijk, C. V. , & Peters, B. A. M. . 1993. Plant-specific soil-borne diseases
contribute to succession in foredune vegetation. Nature, 362(6415), 53-56.
Rieley J O, Wüst R A J, Jauhiainen J, et al. 2008. Tropical peatlands: carbon stores, carbon gas
emissions and contribution to climate change processes[J]. Peatlands & Climate Change, 12, 148-182.
Ringel, & S., M. . 1978. In vitro and in vivo studies of ambruticin (w7783): new class of antifungal
antibiotics. Antimicrobial Agents and Chemotherapy, 13(5), 762-769.
Roesch L F, Fulthorpe R R, Riva A, et al. 2007. Pyrosequencing enumerates and contrasts soil
microbial diversity[J]. Isme Journal, 1(4):283.
Rousk, J. , Brookes, P. C. , & Erland Bååth. 2009. Contrasting soil ph effects on fungal and bacterial
growth suggest functional redundancy in carbon mineralization. Applied & Environmental
Microbiology, 75(6), 1589-96.
Schloss P D, Westcott S L, Ryabin T, et al. 2009. Introducing mothur: Open-Source, Platform-
Independent, Community-Supported Software for Describing and Comparing Microbial
Communities[J]. Applied & Environmental Microbiology, 75(23):7537.
Schmidt S K, Costello E K, Nemergut D R, et al. 2007. Biogeochemical Consequences of Rapid
Microbial Turnover and Seasonal Succession in Soil[J]. Ecology, 88(6):1379-1385.
Segata N, Izard J, Waldron L, et al. 2011. Metagenomic biomarker discovery and explanation[J].
Genome Biology, 12(6):R60.
Sepiah M, Lit R. 2004. Leaf colonising fungi of peat swamp forest. Tropical peat swamps : safe-
guarding a global natural resource: proceedings of the International Conference and Workshop on
Tropical Peat Swamps.
This article is protected by copyright. All rights reserved.

Shen, C. , Xiong, J. , Zhang, H. , Feng, Y. , Lin, X. , & Li, X. , et al. 2013. Soil ph drives the spatial
distribution of bacterial communities along elevation on changbai mountain. Soil Biology and
Biochemistry, 57, 204-211.
Sirikantaramas S, Sugioka N, Lee S.S, Mohamed L, Lee H.S, Szmidt A.E, Yamazaki T 2003.
Molecular identification of ectomycorrhizal fungi associated with Dipterocarpaceae. Tropics 13:69–
77
Slater, L. D., Baird, A. J., Belyea, L. R., Comas, X., & Reeve, A. S. 2009. Carbon cycling in northern
peatlands. Geophysical Monograph,184.
Sorensen K W. 1993. Indonesian peat swamp forests and their role as a carbon sink. Chemosphere, 27,
1065-1082.
Soudzilovskaia N A, Heijden M G A V D, Cornelissen J H C, et al. 2015. Quantitative assessment of
the differential impacts of arbuscular and ectomycorrhiza on soil carbon cycling[J]. New Phytologist,
208(1):280-293
Stams, A. J. M. , Bok, F. A. M. D. , & Luijten, M. L. G. C. . 2002. Biochemical evidence for formate
transfer in syntrophic propionate-oxidizing cocultures of syntrophobacter fumaroxidans and
methanospirillum hungatei. Applied & Environmental Microbiology, 68(9), 4247-4252.
Stockwell CE, Jayarathne T, Cochrane MA et al. 2016. Field measurements of trace gases and
aerosols emitted by peat fires in Central Kalimantan, Indonesia during the 2015 El Niño. Atmospheric
Chemistry and Physics Discussions, 53, 1–37.
Straková P., Niemi, R. M. , Freeman, C. , Peltoniemi, K. , Toberman, H. , & Heiskanen, I. , et al.
2011. Litter type affects the activity of aerobic decomposers in a boreal peatland more than site
nutrient and water table regimes. Biogeosciences,8(9), 2741-2755.
Strickman, R. J. , Fulthorpe, R. R. , Coleman Wasik, J. K. , Engstrom, D. R. , & Mitchell, C. P. . 2016.
Experimental sulfate amendment alters peatland bacterial community structure. Science of the Total
Environment, 566-567, 1289-1296.
This article is protected by copyright. All rights reserved.