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Research Article | Applied and Environmental Science

Shifts in the Bacterial Population and Ecosystem Functions in Response to Vegetation in the Yellow River Delta Wetlands

Jianing Wang, Jingjing Wang, Zheng Zhang, Zhifeng Li, Zhiguo Zhang, Decun Zhao, Lidong Wang, Feng Lu, Yue-zhong Li
Theodore M. Flynn, Editor
Jianing Wang
aState Key Laboratory of Microbial Technology, Institute of Microbial Technology, Shandong University, Qingdao, People’s Republic of China
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Jingjing Wang
aState Key Laboratory of Microbial Technology, Institute of Microbial Technology, Shandong University, Qingdao, People’s Republic of China
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Zheng Zhang
aState Key Laboratory of Microbial Technology, Institute of Microbial Technology, Shandong University, Qingdao, People’s Republic of China
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Zhifeng Li
aState Key Laboratory of Microbial Technology, Institute of Microbial Technology, Shandong University, Qingdao, People’s Republic of China
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Zhiguo Zhang
bSchool of Life Science, Shandong University, Qingdao, People’s Republic of China
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Decun Zhao
cNational Nature Reserve Administration of Yellow River Delta, Dongying, People’s Republic of China
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Lidong Wang
cNational Nature Reserve Administration of Yellow River Delta, Dongying, People’s Republic of China
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Feng Lu
cNational Nature Reserve Administration of Yellow River Delta, Dongying, People’s Republic of China
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Yue-zhong Li
aState Key Laboratory of Microbial Technology, Institute of Microbial Technology, Shandong University, Qingdao, People’s Republic of China
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Theodore M. Flynn
California Department of Water Resources
Roles: Editor
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DOI: 10.1128/mSystems.00412-20
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  • FIG 1
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    FIG 1

    Biogeography characteristics of the bacterial communities in bare and vegetative wetlands of the Yellow River Delta. (a) The geographical sampling locations. Plot A is bare land near the ocean at a distance of ∼2.1 km; plots B and C (at a distance of 2.2 km; the distance between plots A and B is 1.8 km) have sparse Suaeda salsa; plot D (0.7-km distance from plot C) is densely grown with Suaeda salsa; and plot E (1.2-km distance from plot D), which is the sampling site farthest from the ocean, is a grassland of Phragmites communis reeds. Three samples at each plot were collected from different places within a distance of approximately 3 to 5 m (the geographical information and the geomorphology refer to Fig. S1a). Background image was acquired freely from http://www.gscloud.cn/. (b) OTU (97% similarity) numbers in the five plots. (c) Hierarchical clustering tree based on the Bray-Curtis metric at the OTU level. (d) PCoA of OTUs with weighted UniFrac distances. The PERMANOVA data are as follows: for plot A versus plots B/C, F = 12.94, P = 0.014; for plot A versus plots D/E, F = 10.93, P = 0.013; for plots B/C versus plots D/E, F = 7.00, P = 0.003.

  • FIG 2
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    FIG 2

    Bacterial community compositions and their responses to environmental factors in wetlands along the vegetation transition zones in the Yellow River Delta. (a) Bacterial community compositions at the phylum level (“others” = <0.05) of the five plots. (b) Pearson correlation heat map of environmental factors and the relative abundances of the 20 most abundant bacterial phyla in wetland soil samples (*, P < 0.05; **, P < 0.01; ***, P < 0.001). (c) Top 10 predominant bacterial genera in five plots. (d) Relative abundances of the 15 most abundant OTUs of g__norank_c__Gemmatimonadetes in the five plots.

  • FIG 3
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    FIG 3

    Omics analyses of bacterial functions in bare and vegetative wetlands. (a) Relative abundances of microorganisms (bacteria, archaea, eukaryotes, and viruses) in plots A and C based on metagenomic sequencing. (b) The relative abundances of metabolic pathways of plots A and C at KEGG level 3 based on metatranscriptomic sequencing. Each asterisk (*) indicates a fold change value of >2. (c) Volcano plots of the metatranscriptomics-identified genes associated with the main metabolic pathways in plots A and C. (d) Volcano plots of the metatranscriptomics-identified genes associated with the cycling of elements in plots A and C. (e) A phylogenomic tree of MAGs and cultured genomes of the phylum Gemmatimonadetes. (f) Expression patterns of the genes from ydcontigbins.4 in the metatranscriptome. (g) Heat map of the 28 differentially enriched metabolites in the samples of plots A and C using Z-scores [Z = (X − average)/standard deviation].

  • FIG 4
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    FIG 4

    Visualization of proteins identified in both ydcontigbins.4 and metatranscriptomic results and metabolites identified from metabolomics results. TCA cycle components are as follows: SucA, 2-oxoglutarate dehydrogenase E1 component; SucB, 2-oxoglutarate dehydrogenase E2 component; AcnA, aconitate hydratase; PckA, phosphoenolpyruvate carboxykinase; PdhD, dihydrolipoamide dehydrogenase; PdhB, pyruvate dehydrogenase E1 component beta subunit. Purine metabolism components are as follows: PurA, adenylosuccinate synthase; PurD; phosphoribosylamine-glycine ligase; PurF, amidophosphoribosyltransferase; PunA, purine-nucleoside phosphorylase; Pmm-Pgm, phosphomannomutase-phosphoglucomutase; Ndk, nucleoside-diphosphate kinase; YagS, xanthine dehydrogenase YagS FAD-binding subunit. Nicotinate and nicotinamide metabolism components are as follows: PunA, purine-nucleoside phosphorylase; GabD, succinate-semialdehyde dehydrogenase/glutarate-semialdehyde dehydrogenase. Pyruvate metabolism components are as follows: Acs, acetyl coenzyme A (acetyl-CoA) synthetase; PflD, formate C-acetyltransferase P; PckA, phosphoenolpyruvate carboxykinase (ATP); Pps, pyruvate, water dikinase; Pyk, pyruvate kinase; AccC, acetyl-CoA carboxylase, biotin carboxylase subunit; AccD, acetyl-CoA carboxylase carboxyl transferase subunit beta. Type IV pilus components are as follows: PilM, type IV pilus assembly protein PilM; PilB, type IV pilus assembly protein PilB. The type VI secretion system component is as follows: VasG, type VI secretion system protein VasG. Two-component system components are as follows: PhoR, two-component system, OmpR family, phosphate regulon sensor histidine kinase; PhoB, two-component system, OmpR family, alkaline phosphatase synthesis response regulator. Other details are listed in Table S5.

Supplemental Material

  • Figures
  • FIG S1

    Characteristics of plant and soil bacterial alpha diversity in bare and vegetative wetlands of the Yellow River Delta. (a) Close-up views of the sampling sites in the Yellow River Delta. (b) Alpha diversity indices (Ace, Chao1, Shannon, and Simpson) of the plot of bacterial OTUs (97% similarity) from three soil samples at five locations along the vegetation transition zone in the Yellow River Delta. Download FIG S1, TIF file, 2.2 MB.

    Copyright © 2020 Wang et al.

    This content is distributed under the terms of the Creative Commons Attribution 4.0 International license.

  • FIG S2

    Venn diagram of the OTUs (97% similarity) from the five wetland plots of the Yellow River Delta. Download FIG S2, TIF file, 0.4 MB.

    Copyright © 2020 Wang et al.

    This content is distributed under the terms of the Creative Commons Attribution 4.0 International license.

  • FIG S3

    (a and b) Redundancy analysis (RDA) of bacterial communities and environmental parameters at the phylum (a) and family (b) levels. (c and d) Values representing results of the Monte Carlo permutation test performed at the phylum or family level for each physicochemical factor are provided in panels c and d. Download FIG S3, TIF file, 0.6 MB.

    Copyright © 2020 Wang et al.

    This content is distributed under the terms of the Creative Commons Attribution 4.0 International license.

  • TABLE S1

    Geochemical features of 15 soil samples collected from five locations along the vegetation transition zone in the Yellow River Delta. Download Table S1, XLSX file, 0.01 MB.

    Copyright © 2020 Wang et al.

    This content is distributed under the terms of the Creative Commons Attribution 4.0 International license.

  • FIG S4

    Pearson correlation heat map of environmental factors and relative abundances of the 20 most abundant bacterial genera in wetland soil samples (*, P < 0.05; **, P < 0.01; ***, P < 0.001). Download FIG S4, TIF file, 0.5 MB.

    Copyright © 2020 Wang et al.

    This content is distributed under the terms of the Creative Commons Attribution 4.0 International license.

  • TABLE S2

    Predominant bacterial community compositions in each plot at the different taxonomic levels. Download Table S2, XLSX file, 0.02 MB.

    Copyright © 2020 Wang et al.

    This content is distributed under the terms of the Creative Commons Attribution 4.0 International license.

  • TABLE S3

    Metagenomic and metatranscriptomic sequencing information from plot A and C. Download Table S3, XLSX file, 0.04 MB.

    Copyright © 2020 Wang et al.

    This content is distributed under the terms of the Creative Commons Attribution 4.0 International license.

  • TABLE S4

    Abundance of the genes associated with metabolic pathways and cycling of elements retrieved from the 9,969 KEGG orthologs (KOs). Download Table S4, XLSX file, 0.04 MB.

    Copyright © 2020 Wang et al.

    This content is distributed under the terms of the Creative Commons Attribution 4.0 International license.

  • TABLE S5

    Results of annotation of genes from ydcontigbins.4 based on KEGG database. Download Table S5, XLSX file, 0.02 MB.

    Copyright © 2020 Wang et al.

    This content is distributed under the terms of the Creative Commons Attribution 4.0 International license.

  • TABLE S6

    Metabolite information from plots A and C determined using HPLC-MS/MS. Download Table S6, XLSX file, 0.02 MB.

    Copyright © 2020 Wang et al.

    This content is distributed under the terms of the Creative Commons Attribution 4.0 International license.

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Shifts in the Bacterial Population and Ecosystem Functions in Response to Vegetation in the Yellow River Delta Wetlands
Jianing Wang, Jingjing Wang, Zheng Zhang, Zhifeng Li, Zhiguo Zhang, Decun Zhao, Lidong Wang, Feng Lu, Yue-zhong Li
mSystems Jun 2020, 5 (3) e00412-20; DOI: 10.1128/mSystems.00412-20

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Shifts in the Bacterial Population and Ecosystem Functions in Response to Vegetation in the Yellow River Delta Wetlands
Jianing Wang, Jingjing Wang, Zheng Zhang, Zhifeng Li, Zhiguo Zhang, Decun Zhao, Lidong Wang, Feng Lu, Yue-zhong Li
mSystems Jun 2020, 5 (3) e00412-20; DOI: 10.1128/mSystems.00412-20
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KEYWORDS

soil bacterial composition
cyanobacteria
Gemmatimonadetes
omics analyses
carbon cycling
estuarine coastal wetland
Yellow River Delta

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