Spatial Distribution of Bacterial Communities in High-Altitude Freshwater Wetland Sediment

Spatial distribution of bacterial communities in high-altitude freshwater wetland sediment

Yong Liu, Jingxu Zhang, Lei Zhao, Xiaoling Zhang & Shuguang Xie

Limnology The Japanese Society of Limnology

ISSN 1439-8621 Volume 15 Number 3

Limnology (2014) 15:249-256 DOI 10.1007/s10201-014-0429-0

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1 23 Author's personal copy

Limnology (2014) 15:249–256 DOI 10.1007/s10201-014-0429-0

RESEARCH PAPER

Spatial distribution of bacterial communities in high-altitude freshwater wetland sediment

Yong Liu • Jingxu Zhang • Lei Zhao • Xiaoling Zhang • Shuguang Xie

Received: 27 January 2014 / Accepted: 27 March 2014 / Published online: 12 April 2014 Ó The Japanese Society of Limnology 2014

Abstract Sediment microorganisms play a crucial role in Keywords Aquatic ecosystem Microbial community a variety of biogeochemical processes in freshwater eco- Proteobacteria Wetland Sediment Freshwater systems. The objective of the current study was to investigate the spatial distribution of sediment bacterial community structure in Luoshijiang Wetland, located in Introduction Yunnan–Kweichow Plateau (China). Wetland sediments at different sites and depths were collected. Clone library Aquatic sediment shelters a complex microbial ecosystem analysis indicates bacterial communities varied with both which is composed of high densities of viable microor- sampling site and sediment depth. A total of fourteen bac- ganisms (Martins et al. 2011). A sediment microbial terial phyla were identified in sediment samples, including community might be involved in a variety of biogeo- Proteobacteria, Acidobacteria, Actinobacteria, Armatimo- chemical processes, such as decomposition of organic nadetes, Bacteroidetes, Chlorobi, Chloroflexi, Cyanobac- matter, methane production, nitrification, denitrification, teria, Firmicutes, Gemmatimonadetes, Nitrospirae, sulfur oxidation, sulphate reduction, phosphorus uptake/ Planctomycetes, Spirochaetes, and Verrucomicrobia. Pro- release, and iron reduction (Martins et al. 2011; Song teobacteria (mainly Betaproteobacteria and Deltaproteo- et al. 2012; Cheng et al. 2013). Sediment microbial bacteria) predominated in wetland sediments. Moreover, community structure can be influenced by many envi- the proportions of Alphaproteobacteria, Acidobacteria, ronmental factors, such as salinity, organic matter and Bacteroidetes, Gemmatimonadete, and Planctomycetes nutrients (Ye et al. 2009; Ribeiro et al. 2013), yet the were significantly correlated with chemical properties. links between sediment microbial community and environmental conditions remain largely unclear. Different environmental niches can exist in benthic sediments even on a millimeter scale (Spring et al. 2000), which can result in a spatial variation of sediment microbial com- Handling Editor: Hisaya Kojima. munity structure (Song et al. 2012; Cheng et al. 2013). In addition, sediment is a stratified habitat where substrates Electronic supplementary material The online version of this article (doi:10.1007/s10201-014-0429-0) contains supplementary and electron acceptors essential for microorganisms are material, which is available to authorized users. gradually scavenged, which also provides niches for metabolically diverse microorganisms (Zhao et al. 2008). Y. Liu L. Zhao However, information on the depth-related change of Yunnan Key Laboratory of Pollution Process and Management of Plateau Lake-Watershed, Kunming 650034, China sediment microbial community structure is still very limited. To date, few previous studies have investigated Y. Liu J. Zhang X. Zhang S. Xie (&) the depth-related change of bacterial community structure College of Environmental Sciences and Engineering, The Key in lake sediment (Zhao et al. 2008; Ye et al. 2009; Zeng Laboratory of Water and Sediment Sciences (Ministry of Education), Peking University, Beijing 100871, China et al. 2009; Liu et al. 2010; Shivaji et al. 2011), and in e-mail: [email protected] reservoir sediment (Qu et al. 2008). 123 Author's personal copy

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Wetlands play a number of eco-environmental roles. To Laboratories). The same amount of DNA from triplicate date, the structures of microbial communities in wetland soils samples was pooled together for clone library analysis. and sediments have been extensively investigated (Jiang Bacterial 16S rRNA genes were amplified using primers et al. 2013; Peralta et al. 2013), which has contributed to our 27F (50-GAGTTTGATCMTGGCTCAG-30) and 1492R understanding of the complex biological processes within (50-GGTTACCTTGTTACGACTT-30) according to the wetland ecosystems. However, the depth-related change of literature (Zhang et al. 2012a). PCR products were cloned bacterial community structure in wetland sediment remains into pMD19-T vector (Takara Corp, Japan) with ampicillin unclear. Moreover, little is known about bacterial commu- selection and blue/white screening. The clones containing nities in freshwater wetland sediment and their spatial vari- correct sizes were sequenced at SinoGenoMax Co., Ltd. ation (Wang et al. 2012). Information on sediment bacterial In this study, partial 16S rRNA gene sequences (about community structure in high-altitude freshwater wetlands is 800 bp) were used for analyses. The Ribosomal Database still lacking. The Luoshijiang Wetland is a freshwater wet- Project analysis tool ‘‘classifier’’ (http://rdp.cme.msu.edu/ land in the Yunnan-Kweichow Plateau. The freshwater classifier/classifier.jsp) was applied to determine the taxo- wetland is adjacent to the Rrhai Lake, the second largest nomic identity of the sequence obtained in this study high-altitude lake in Yunnan Province (China). It covers an (Wang et al. 2007). Principal components analysis (PCA) area of about 1 km2 with an elevation of about 2,056 m. using the software package CANOCO for Windows 4.5 Annual mean air temperature and annual precipitation in the was performed on a correlation matrix composed of the local region were 15.7 °C, and 1,000–1,200 mm, respec- relative abundances of the identified bacterial groups from tively (Zhang et al. 2013). In the present study, the objective eight individual sediment samples, to explore the vari- was to investigate the spatial distribution of sediment bac- ability of bacterial community composition. In addition, terial community structure in Luoshijiang Wetland. Pearson’s correlation analysis of the identified bacterial groups with chemical parameters was performed using SPSS 20.0 software. The bacterial sequences obtained in Materials and methods this study were submitted to GenBank under accession numbers KF247431–KF247993. Sampling sites and sample collection

Wetland sediment samples were collected in triplicate using a Results core sampler at four different sites in Luoshijiang Wetland: A (25°5702500N–100°0600600E, no vegetation zone), B (5°5701200 Phylum composition N–100°0505900E, reed-planted zone), C (25°570400N– 100°0600000E, densely water-lily-planted zone), and D A total of 66, 84, 77, 72, 59, 75, 66 and 64 bacterial (25°5605500N–100°0505900E, sparsely water-lily-planted sequences were retrieved from samples AU, AL, BU, BL, zone). The schematic representation of the sampling sites and CU, CL, DU and DL, respectively. The rarefaction curves the environmental conditions of the water body measured for each bacterial clone library did not level off (Fig. S1). directly above the sediment at the time of sampling has been The percentage of coverage for each sample ranged roughly described in detail in a previous study (Zhang et al. 2013). between 50 and 60 % (data not shown). These results For each site, sediment samples were sliced into layers. suggested that further sequencing would result in more During this study, the upper layer (0–5 cm) and the lower operational taxonomic units (OTUs). Bacterial community layer (10–15 cm) were used for further analysis. The upper compositions of the eight sediment samples are shown in layer and lower layer sediments in sampling sites A–D Fig. 1. Unclassified bacterial sequences had a very high were referred to as samples AU and AL, BU and BL, CU proportion (28.8–40.6 %) in samples BL, DU and DL, but and CL, and DU and DL, respectively. were less abundant in other samples. In this study, a total of ? Total organic carbon (TOC), ammonium nitrogen (NH4 - 14 known phyla were identified in these samples, including N), total nitrogen (TN), available phosphorus (AP), and total Proteobacteria, Acidobacteria, Actinobacteria, Armatimo- phosphorus (TP) contents of the sediments were 2.01–6.17, nadetes, Bacteroidetes, Chlorobi, Chloroflexi, Cyanobac- 0.11–0.36, 0.22–2.44, 0.01–0.05, and 0.25–0.73 g/kg, teria, Firmicutes, Gemmatimonadetes, Nitrospirae, respectively (Table S1). Planctomycetes, Spirochaetes, and Verrucomicrobia, while only Proteobacteria and Acidobacteria were shared among Bacterial clone library analysis all the eight sediment samples. Proteobacteria predominated in each sample (with a relative abundance of Total genomic DNA of each sediment sample was 51.5–76.6 %). However, except at sampling site D, the extracted using a Powersoil DNA extraction kit (Mobio composition of major proteobacterial classes (with relative 123 Author's personal copy

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Fig. 1 Comparison of the 100% Unclassified bacteria quantitative contribution of the Verrucomicrobia 90% sequences affiliated with Spirochaetes different phyla and subphyla to 80% Planctomycetes the total number of sequences Nitrospirae from the eight samples. 70% Gemmatimonadetes Sequences not classified to any Firmicutes known phylum are included as 60% Cyanobacteria unclassified bacteria Chloroflexi 50% Chlorobi 40% Bacteroidetes Armatimonadetes 30% Actinobacteria Relative abundance Acidobacteria 20% Unclassified Proteobacteria Epsilonproteobacteria 10% Deltaproteobacteria Gammaproteobacteria 0% AU AL BU BL CU CL DU DL Betaproteobacteria Alphaproteobacteria Sample abundance C5 %) and their proportions differed greatly in with available phosphorus and total phosphorus (p \ 0.05). upper layer sediment and lower layer sediment. For exam- However, other proteobacterial groups did not show any ple, at sampling site A, the major proteobacterial classes in significant correlation with the determined sediment the upper layer were Deltaproteobacteria (18.2 %), Beta- chemical parameters. Acidobacteria had a significant proteobacteria (16.7 %), Alphaproteobacteria (12.1 %), positive correlation with total phosphorus (p \ 0.05). In and Epsilonproteobacteria (9.1 %), while the lower layer addition, Bacteroidetes was positively correlated with total was mainly composed of Betaproteobacteria (36.9 %), phosphorus (p \ 0.05), but negatively with total nitrogen Deltaproteobacteria (20.2 %), and Gammaproteobacteria and total organic carbon (p \ 0.05). (7.1 %). These results illustrate a depth-related change of proteobacterial community structure in wetland sediment. Genus composition Moreover, a large variation of proteobacterial community structure with sampling site was also observed. Acidobac- For sample AU, a large portion of sequences (39/66) could teria was the second most important bacterial group, with a be classified at genus level. In contrast, in the other wetland relative abundance of 4.5–15.2 % in each sample. It was sediment samples, less than half of the sequences could be much more abundant in samples AU and CU. Bacteroidetes related to the known genera. Table 2 illustrates the abun- was also a commonly detected bacterial group. It showed a dance and distribution of the 55 identified genera detected large abundance in sample CU (10.2 %), but was much less in the eight sediment samples. No single genus was abundant in the other samples (0–6.9 %). detected among all the eight wetland sediment samples. Principal components analysis applied to sediment Most genera appeared only in one or two samples. Sample bacterial community composition shows that the PCA1 and DU and DL showed a marked difference in genus com- PCA2 axes together explained 85.1 % of the total vari- position. Therefore, at the genus level of taxonomic clas- ability of the variables included in the analysis (Fig. 2). sification, variations of bacterial community structure Samples AU, BU, CU and DU were distant from each among the eight sediment samples became more evident. other. A similar distribution pattern was found among samples AL, BL, CL and DL. These results confirmed that sediment bacterial community structure could be affected Discussion by sampling site. Moreover, the upper layer samples were generally not grouped with the lower layer ones. Therefore, Proteobacteria might be involved in various biogeochem- sediment bacterial community structure could be depen- ical processes in freshwater sediment (Cheng et al. 2013). dent on sampling site and sediment depth. Table 1 illus- The predominance of Proteobacteria in sediments has been trates the Pearson’s correlation coefficients for the usually found in various freshwater ecosystems, such as relationship between the proportion change of the known lake (Spring et al. 2000; Liu et al. 2010; Song et al. 2012), bacterial groups and sediment chemical properties. Al- and reservoir (Qu et al. 2008; Roske et al. 2012; Cheng phaproteobacteria showed a significant positive correlation et al. 2013). These previous studies indicated that the

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Fig. 2 Two-dimensional PCA ordination of the identiﬁed phylum and proteobacterial classes described in Fig. 1

Table 1 Pearson’s correlation ? Bacterial groups TN (g/kg) NH4 -N (g/kg) TP (g/kg) AP (g/kg) TOC (g/kg) coefficients describing the relationship between water Alphaproteobacteria -0.02 0.27 0.75* 0.81* -0.02 characteristics and the Betaproteobacteria -0.16 0.44 0.24 0.15 0.17 proportion change of major bacterial groups Gammaproteobacteria -0.45 -0.2 0.35 0.06 -0.27 Deltaproteobacteria 0.16 -0.46 -0.56 -0.65 -0.03 Epsilonproteobacteria 0.61 0.15 -0.39 0.14 0.35 Acidobacteria 0 0.27 0.79* 0.69 0.05 Actinobacteria 0.11 0.46 0.48 0.8* 0.15 Armatimonadetes 0.7 0.09 -0.69 -0.3 0.51 Bacteroidetes -0.75* -0.69 0.73* -0.11 -0.74* Chlorobi -0.54 -0.46 0.68 -0.02 -0.55 Chloroflexi -0.29 -0.1 0.296 -0.28 -0.11 Cyanobacteria -0.53 -0.64 0.5 -0.23 -0.63 Firmicutes -0.05 0 0.12 0.4 -0.19 Gemmatimonadetes 0.31 0.6 0.44 0.95* 0.31 Nitrospira -0.22 0.35 -0.04 -0.1 0 Planctomycetes 0.44 0.81* 0.21 0.75* 0.57 Spirochaetes -0.19 -0.28 -0.22 -0.16 -0.31 * Correlation is significant at the Verrucomicrobia 0.01 0.53 0.24 0.49 0.25 0.05 level composition of major proteobacterial classes and their Betaproteobacteria and Deltaproteobacteria. The domi- proportions could have a large variation in sediments from nance of Betaproteobacteria as well as Deltaproteobacte- different freshwater ecosystems. To date, information on ria was also found in sediments of Saidenbach reservoir the structures of microbial communities in wetland sedi- (Germany) (Roske et al. 2012). In addition, Epsilonprote- ments is still very limited (Jiang et al. 2013). To the obacteria was usually the minor member of proteobacterial authors’ knowledge, this was the first study on bacterial communities in sediments (Song et al. 2012; Roske et al. community composition of freshwater wetland sediment. 2012). However, in this study, the abundance of Epsilon- In this study, the predominance of Proteobacteria was proteobacteria was found in three wetland sediment found in sediments of a high-altitude freshwater wetland. samples. Although phylum Verrucomicrobia predominated in the Previous studies have shown that the proportions of the water body in the Luoshijiang Wetland (Zhang et al. 2013), different proteobacterial subdivisions in sediment varied it became a minor group in the sediment samples. The with sampling sites (Song et al. 2012; Cheng et al. 2013). proteobacterial communities were mainly composed of In this study, a shift of proteobacterial community structure

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Table 2 Distribution of the sequences affiliated with the identified bacterial genera in the eight sediment samples Phylogenetic affiliation AU AL BU BL CU CL DU DL

Alphaproteobacteria Dongia 1––––––– Roseomonas 1–––1––– Hyphomicrobium 2––––––– Methylocystis –1–2–––– Rhodoplanes ––1––––– Deﬂuviicoccus ––––1––– Bauldia –––––1–– Betaproteobacteria Dechloromonas 1–1––––– Sulfuricella 11–––––– Thiobacillus –56––8–– Curvibacter ––2––––– Limnohabitans –––1–––– Comamonas –––––––1 Gammaproteobacteria Pseudomonas 2––––––– Steroidobacter –21––1–– Methylobacter ––242––– Methylococcus ––––––1– Haliea ––––––1– Deltaproteobacteria Smithella 1–1––21– Geobacter 2––112–2 Cystobacter 1––––––– Desulfomonile –1–––––– Anaeromyxobacter –1–––1–– Desulfobacterium ––4–4––– Syntrophorhabdus –––1–––– Desulfobulbus ––––1––– Koﬂeria ––––1––– Syntrophus ––––––3– Epsilonproteobacteria Sulfuricurvum 6–––2–68 Acidobacteria Gp6 233––31– Gp17 2–––41–– Gp23 1–––1––– Gp3 2221––2– Gp11 2––––––– Gp18 11–––1 3 Gp22 –2––1––– Gp7 ––1–1––– Gp19 –––1–––– Gp10 ––––1––– Actinobacteria Ilumatobacter 2––––––– Arthrobacter –1––––––

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Table 2 continued Phylogenetic afﬁliation AU AL BU BL CU CL DU DL

Armatimonadetes Armatimonadetes_gp2 –––––––1 Bacteroidetes Flavobacterium –1–––––– Terrimonas –1–––––– Flavisolibacter –––––1–– Cyanobacteria GpXIII ––––2––– Bacillariophyta ––––––1– Firmicutes Pasteuria 1–––––1– Clostridium sensu stricto 4 – – – – – 3 – Desulfosporosinus ––––––1– Pelotomaculum ––––––2– Saccharofermentans –––1––1– Gemmatimonadetes Gemmatimonas 21–––––– Nitrospirae Nitrospira –1–––11– Planctomycetes Gemmata 2–1––––– Total 39 4 25 12 23 22 25 15 –, not detected was also observed at different sampling sites in Luoshiji- phosphorus, while Firmicutes showed a significant positive ang Wetland. Few previous studies have investigated the correlation with total nitrogen (Cheng et al. 2013). In this depth-related change of bacterial community structure in study, the chemical features of wetland sediment samples lake sediment. Zhao et al. (2008) found that sediment were very different. Pearson’s correlation analysis illus- bacterial community structure in Lake Taihu (China) var- trates that the relative abundances of Alphaproteobacteria, ied with the increase of sediment depth. They further Acidobacteria, Bacteroidetes, Gemmatimonadete,or suggested that some bacteria could be suppressed or Planctomycetes were significantly correlated with one or a stimulated as a function of depth. Another two studies also few environmental parameters. However, Betaproteobac- showed the bacterial community change with sediment teria and Deltaproteobacteria, as the two largest proteo- depth in Lake Taihu (Zeng et al. 2009; Liu et al. 2010), bacterial components in sediments of Luoshijiang Wetland, while Ye et al. (2009) indicated that bacterial communities did not show significant correlation with the determined in different sediment layers in Lake Taihu were very environmental parameters. Our previous study also showed similar. Stratification of bacteria with sediment depth was that some major bacterial groups did not show any sig- observed in a freshwater lake in Antarctica (Shivaji et al. nificant correlation with reservoir sediment chemical 2011). However, little is known about the relationship properties (Cheng et al. 2013). Therefore, further efforts between bacterial community and sediment depth in other will be necessary in order to elucidate the links between types of freshwater ecosystems. In this study, a marked sediment bacterial community structure and depth-related difference of bacterial community structures was usually gradient of geochemical properties. found in different sediment layers in Luoshijiang Wetland. Microorganisms from gammaproteobacterial genera Previous studies indicated sediment bacterial commu- Methylobacter and Methylococcus are known for oxida- nity structure in freshwaters can be affected by organic tion of one-carbon compounds, most notably methane matter and nutrients (Ye et al. 2009; Ribeiro et al. 2013; (Tsutsumi et al. 2011; Kleiveland et al. 2012). Members of Song et al. 2012). Our previous study indicated that, in alphaproteobacterial genera Methylocystis and Hypho- reservoir sediments, Gammaproteobacteria and Deltapro- microbium are capable of growth on multi-carbon com- teobacteria had a significant negative correlation with total pounds and can degrade chlorinated hydrocarbons 123 Author's personal copy

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(Nikolausz et al. 2005; Vuilleumier et al. 2011; Jagadevan References and Semrau 2013). Members of genera Comamonas (Betaproteobacteria), Pseudomonas (Gammaproteobacte- Abicht HK, Mancini S, Karnachuk OV, Solioz M (2011) Genome ria), and Arthrobacter (Actinobacteria) can degrade a sequence of Desulfosporosinus sp. OT, an acidophilic sulfate- reducing bacterium from copper mining waste in Norilsk, variety of environmental organic pollutants (Ruzicka et al. Northern Siberia. J Bacteriol 193(21):6104–6105 2011; Dellai et al. 2013; Tribedi and Sil 2013; Wang et al. Ahn YB, Chae JC, Zylstra GJ, Haggblom MM (2009) Degradation of 2013; Zhou et al. 2013). In addition, Steroidobacter phenol via phenylphosphate and carboxylation to 4-hydroxy- (Gammaproteobacteria) is known for anaerobic degrada- benzoate by a newly isolated strain of the sulfate-reducing bacterium Desulfobacterium aniline. 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