Abstract
Symbiotic microbiomes of Sphagnum have been confirmed to play a fundamental role in carbon and nitrogen cycles, however, little is known about microbiomes associated with other bryophytes in subtropical peatland ecosystems. To explore the differences in community structure, metabolic potential and interaction relationship of bacterial microbiomes associated with different bryophytes species, the gametophytes of three bryophyte species (Sphagnum palustre, Aulacomnium androgynum, and Polytrichum commune) and their underlying peat sediments were collected from the subtropical Dajiuhu Peatland and subjected to Illumina high-throughout sequencing of 16S rRNA gene. Results showed that bacterial diversity was lowest in S. palustre, the dominant moss species, among the three moss species investigated in Dajiuhu Peatland. Bacterial communities from bryophytes clearly separated with those from sediments as indicated by both phylogenetic and taxonomical approaches. Linear discriminant analysis effect size (LEfSe) identified 30 and 36 indicator taxa in mosses and peat sediments. Bacteroidetes, Verrucomicrobia and Thermoleophilia significantly enriched in S. palustre, A. androgynum and P. commune, Chloroflexi, Proteobacteria and Acidobacteria subgroup 6 was indicator taxa for corresponding underlying sediments, respectively. Despite of these differences in compositions, bacterial functional structures were similar among all bryophytes, such as abundant aerobic heterotrophs, rare nitrifiers and denitrifiers. This phenomenon was also observed among the underlying sediments. Network analysis indicated that Proteobacteria and Acidobacteria located in the center of network and exerted strong interactions to other taxa. The sub-network of bacterial communities in sediments was more connected and microbial groups were more competitive than those in bryophytes subnetwork. Our results offer new insight into the community structure, ecological function and interaction pattern of bacterial microbiomes in the Dajiuhu Peatland across different habitats.
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References Cited
Barabási, A. L., 2009. Scale-Free Networks: A Decade and Beyond. Science, 325(5939): 412–413. https://doi.org/10.1126/science.1173299
Bassett, D. S., Bullmore, E., 2006. Small-World Brain Networks. The Neuroscientist, 12(6): 512–523. https://doi.org/10.1177/1073858406293182
Bauer, I. E., Tirlea, D., Bhatti, J. S., et al., 2007. Environmental and Biotic Controls on Bryophyte Productivity along Forest to Peatland Ecotones. Canadian Journal of Botany, 85(5): 463–475. https://doi.org/10.1139/b07-045
Beck, M., 2017. Ggord: Ordination Plots with ggplot2. R Package Version 1.0.0
Becking, J. H., 2006. The Genus Beijerinckia. In: Dworkin, M., Falkow, S., Rosenberg, E., et al., eds., The Prokaryotes. Springer, New York. 151–162. https://doi.org/10.1007/0-387-30745-1_8
Berry, D., Widder, S., 2014. Deciphering Microbial Interactions and Detecting Keystone Species with Co-Occurrence Networks. Frontiers in Microbiology, 5: 219. https://doi.org/10.3389/finicb.2014.00219
Bragina, A., Berg, C., Cardinale, M., et al., 2012. Sphagnum Mosses Harbour Highly Specific Bacterial Diversity during Their Whole Lifecycle. The ISME Journal, 6(4): 802–813. https://doi.org/10.1038/ismej.2011.151
Bragina, A., Berg, C., Müller, H., et al., 2013a. Insights into Functional Bacterial Diversity and Its Effects on Alpine Bog Ecosystem Functioning. Scientific Reports, 3: 1955. https://doi.org/10.1038/srep01955
Bragina, A., Cardinale, M., Berg, C., et al., 2013b. Vertical Transmission Explains the Specific Burkholderia Pattern in Sphagnum Mosses at Multi-Geographic Scale. Frontiers in Microbiology, 4: 394. https://doi.org/10.3389/fmicb.2013.00394
Caporaso, J. G., Kuczynski, J., Stombaugh, J., et al., 2010. QIIME Allows Analysis of High-Throughput Community Sequencing Data. Nature Methods, 7(5): 335–336. https://doi.org/10.1038/nmeth.fi.303
Chao, A., Chazdon, R. L., Colwell, R. K., et al., 2005. A New Statistical Approach for Assessing Compositional Similarity Based on Incidence and Abundance Data. Ecology Letters, 8(2): 148–159. https://doi.org/10.1111/j.1461-0248.2004.00707.x
Chen, X., Bu, Z. J., Wang, S. Z., et al., 2009. Niches of Seven Bryophyte Species in Hani Peat Land of Changbai Mountains. Chinese Journal of Applied Ecology, 20(3): 574–578 (in Chinese with English Abstract)
Claesson, M. J., O’Sullivan, O., Wang, Q., et al., 2009. Comparative Analysis of Pyrosequencing and a Phylogenetic Microarray for Exploring Microbial Community Structures in the Human Distal Intestine. PLoS One, 4(8): e6669. https://doi.org/10.1371/journal.pone.0006669
Clauset, A., Shalizi, C. R., Newman, M. E. J., 2009. Power-Law Distributions in Empirical Data. SIAM Review, 51(4): 661–703. https://doi.org/10.1137/070710111
Dai, Z. M., Su, W. Q., Chen, H. H., et al., 2018. Long-Term Nitrogen Fertilization Decreases Bacterial Diversity and Favors the Growth of Actinobacteria and Proteobacteria in Agro-Ecosystems across the Globe. Global Change Biology, 24(8): 3452–3461. https://doi.org/10.1111/gcb.14163
Deng, Y. C., Cui, X. Y., Hernańdez, M., et al., 2014. Microbial Diversity in Hummock and Hollow Soils of Three Wetlands on the Qinghai-Tibetan Plateau Revealed by 16S rRNA Pyrosequencing. PLoS One, 9(7): e103115. https://doi.org/10.1371/journal.pone.0103115
Dodds, W. K., Gudder, D. A., Mollenhauer, D., 1995. The Ecology of Nostoc. Journal of Phycology, 31(1): 2–18. https://doi.org/10.1111/j.0022-3646.1995.00002.x
Edgar, R. C., 2013. UPARSE: Highly Accurate OTU Sequences from Microbial Amplicon Reads. Nature Methods, 10(10): 996–998. https://doi.org/10.1038/nmeth.2604
Elumeeva, T. G., Soudzilovskaia, N. A., During, H. J., et al., 2011. The Importance of Colony Structure versus Shoot Morphology for the Water Balance of 22 Subarctic Bryophyte Species. Journal of Vegetation Science, 22(1): 152–164. https://doi.org/10.1111/j.1654-1103.2010.01237.x
Faith, D. P., 1992. Conservation Evaluation and Phylogenetic Diversity. Biological Conservation, 61(1): 1–10. https://doi.org/10.1016/0006-3207(92)91201-3
Faust, K., Raes, J., 2016. CoNet App: Inference of Biological Association Networks Using Cytoscape. F1000Research, 5: 1519. https://doi.org/10.12688/f1000research.9050.2
George, D., Mallery, P., 1998. SPSS for Windows Step by Step: A Simple Guide and Reference. Allyn & Bacon, Boston
Graham, D. W., Chaudhary, J. A., Hanson, R. S., et al., 1993. Factors Affecting Competition between Type I and Type II Methanotrophs in Two-Organism, Continuous-Flow Reactors. Microbial Ecology, 25(1): 1–17. https://doi.org/10.1007/BF00182126
Grime, J. P., 1973. Competitive Exclusion in Herbaceous Vegetation. Nature, 242(5396): 344–347. https://doi.org/10.1038/242344a0
Hill, T. C. J., Walsh, K. A., Harris, J. A., et al., 2003. Using Ecological Diversity Measures with Bacterial Communities. FEMS Microbiology Ecology, 43(1): 1–11. https://doi.org/10.1016/S0168-6496(02)00449-X
Holden, J., 2006. Peatland Hydrology. In: Martini, I. P., Martínez Cortizas, A., Chesworth, W., eds., Peatlands: Evolution and Records of Environmental and Climate Changes. Elsevier, Amsterdam. 319–346
Huang, X. Y., Zhang, Z. Q., Wang, H. M., et al., 2017. Overview on Critical Zone Observatory at Dajiuhu Peatland, Shennongjia. Earth Science, 42(6): 1026–1038 (in Chinese with English Abstract)
Huang, Y. B., Zhao, T. T., Xiang, W., et al., 2021. Stability of Organic Iron Complexes in Dajiuhu Peats and Its Ecological Significance. Earth Science, (5): 1862–1870. https://doi.org/10.3799/dqkx.2020.149 (in Chinese with English Abstract)
Hughes, J. B., Hellmann, J. J., Ricketts, T. H., et al., 2001. Counting the Uncountable: Statistical Approaches to Estimating Microbial Diversity. Applied and Environmental Microbiology, 67(10): 4399–4406. https://doi.org/10.1128/AEM.67.10.4399-4406.2001
Hunter, P. R., Gaston, M. A., 1988. Numerical Index of the Discriminatory Ability of Typing Systems: An Application of Simpson’s Index of Diversity. Journal of Clinical Microbiology, 26(11): 2465–2466. https://doi.org/10.1128/jcm.26.11.2465-2466.1988
Jiang, X. T., Peng, X., Deng, G. H., et al., 2013. Illumina Sequencing of 16S rRNA Tag Revealed Spatial Variations of Bacterial Communities in a Mangrove Wetland. Microbial Ecology, 66(1): 96–104. https://doi.org/10.1007/s00248-013-0238-8
Kostka, J. E., Weston, D. J., Glass, J. B., et al., 2016. The Sphagnum Microbiome: New Insights from an Ancient Plant Lineage. The New Phytologist, 211(1): 57–64. https://doi.org/10.1111/nph.13993
Kumar, R., Novak, J., Tomkins, A., 2010. Structure and Evolution of Online Social Networks. Link Mining: Models, Algorithms, and Applications. Springer, New York. 337–357. https://doi.org/10.1007/978-1-4419-6515-8_13
Kuykendall, L. D., 2015. Bradyrhizobium. Bergey’s Manual of Systematics of Archaea and Bacteria. John Wiley & Sons, New Jersey. 1–11
Lau, E., Nolan Iv, E., Dillard, Z. W., et al., 2015. High Throughput Sequencing to Detect Differences in Methanotrophic Methylococcaceae and Methylocystaceae in Surface Peat, Forest Soil, and Sphagnum Moss in Cranesville Swamp Preserve, West Virginia, USA. Microorganisms, 3(2): 113–136. https://doi.org/10.3390/microorganisms3020113
León, C. A., Oliván, G., Larraín, J., et al., 2014. Bryophytes and Lichens in Peatlands and Tepualia Stipularis Swamp Forests of Isla Grande de Chiloé (Chile). Anales Del Jardín Botánico De Madrid, 71(1): e003. https://doi.org/10.3989/ajbm.2342
Levy-Booth, D. J., Prescott, C. E., Grayston, S. J., 2014. Microbial Functional Genes Involved in Nitrogen Fixation, Nitrification and Denitrification in Forest Ecosystems. Soil Biology and Biochemistry, 75: 11–25. https://doi.org/10.1016/j.soilbio.2014.03.021
Lima-Mendez, G., Faust, K., Henry, N., et al., 2015. Determinants of Community Structure in the Global Plankton Interactome. Science, 348(6237): e1262073. https://doi.org/10.1126/science.1262073
Louca, S., Parfrey, L. W., Doebeli, M., 2016. Decoupling Function and Taxonomy in the Global Ocean Microbiome. Science, 353(6305): 1272–1277. https://doi.org/10.1126/science.aaf4507
Ma, B., Wang, H. Z., Dsouza, M., et al., 2016. Geographic Patterns of Co-Occurrence Network Topological Features for Soil Microbiota at Continental Scale in Eastern China. The ISME Journal, 10(8): 1891–1901. https://doi.org/10.1038/ismej.2015.261
Magoč, T., Salzberg, S. L., 2011. FLASH: Fast Length Adjustment of Short Reads to Improve Genome Assemblies. Bioinformatics, 27(21): 2957–2963. https://doi.org/10.1093/bioinformatics/btr507
Maksimova, V., Klavina, L., Bikovens, O., et al., 2013. Structural Characterization and Chemical Classification of some Bryophytes Found in Latvia. Chemistry & Biodiversity, 10(7): 1284–1294. https://doi.org/10.1002/cbdv.201300014
Mellegård, H., Stalheim, T., Hormazabal, V., et al., 2009. Antibacterial Activity of Sphagnum Acid and other Phenolic Compounds Found in Sphagnum Papillosum Against Food-Borne Bacteria. Letters in Applied Microbiology, 49(1): 85–90. https://doi.org/10.1111/j.1472-765X.2009.02622.x
Opelt, K., Berg, G., 2004. Diversity and Antagonistic Potential of Bacteria Associated with Bryophytes from Nutrient-Poor Habitats of the Baltic Sea Coast. Applied and Environmental Microbiology, 70(11): 6569–6579. https://doi.org/10.1128/AEM.70.11.6569-6579.2004
Opelt, K., Chobot, V., Hadacek, F., et al., 2007. Investigations of the Structure and Function of Bacterial Communities Associated with Sphagnum Mosses. Environmental Microbiology, 9(11): 2795–2809. https://doi.org/10.1111/j.1462-2920.2007.01391.x
Putkinen, A., Larmola, T., Tuomivirta, T., et al., 2014. Peatland Succession Induces a Shift in the Community Composition of Sphagnum-Associated Active Methanotrophs. FEMS Microbiology Ecology, 88(3): 596–611. https://doi.org/10.1111/1574-6941.12327
Raghoebarsing, A. A., Smolders, A. J. P., Schmid, M. C., et al., 2005. Methanotrophic Symbionts Provide Carbon for Photosynthesis in Peat Bogs. Nature, 436(7054): 1153–1156. https://doi.org/10.1038/nature03802
Rauha, J. P., Remes, S., Heinonen, M., et al., 2000. Antimicrobial Effects of Finnish Plant Extracts Containing Flavonoids and other Phenolic Compounds. International Journal of Food Microbiology, 56(1): 3–12. https://doi.org/10.1016/S0168-1605(00)00218-X
Segata, N., Izard, J., Waldron, L., et al., 2011. Metagenomic Biomarker Discovery and Explanation. Genome Biology, 12(6): R60. https://doi.org/10.1186/gb-2011-12-6-r60
Shannon, P., Markiel, A., Ozier, O., et al., 2003. Cytoscape: A Software Environment for Integrated Models of Biomolecular Interaction Networks. Genome Research, 13(11): 2498–2504. https://doi.org/10.1101/gr.1239303
Shcherbakov, A. V., Bragina, A. V., Kuzmina, E. Y., et al., 2013. Endophytic Bacteria of Sphagnum Mosses as Promising Objects of Agricultural Microbiology. Microbiology, 82(3): 306–315. https://doi.org/10.1134/S0026261713030107
Silverman, J. D., Washburne, A. D., Mukherjee, S., et al., 2017. A Phylogenetic Transform Enhances Analysis of Compositional Microbiota Data. eLife, 6: e21887. https://doi.org/10.7554/eLife.21887
Spearing, A. M., 1972. Cation-Exchange Capacity and Galacturonic Acid Content of Several Species of Sphagnum in Sandy Ridge Bog, Central New York State. The Bryologist, 75(2): 154–158. https://doi.org/10.2307/3241443
Sun, H., Terhonen, E., Koskinen, K., et al., 2014. Bacterial Diversity and Community Structure along Different Peat Soils in Boreal Forest. Applied Soil Ecology, 74(2): 37–45. https://doi.org/10.1016/j.apsoil.2013.09.010
Tang, J. Y., Ma, J., Li, X. D., et al., 2016. Illumina Sequencing-Based Community Analysis of Bacteria Associated with Different Bryophytes Collected from Tibet, China. BMC Microbiology, 16(1): 276. https://doi.org/10.1186/s12866-016-0892-3
Tarnocai, C., Canadell, J. G., Schuur, E. A. G., et al., 2009. Soil Organic Carbon Pools in the Northern Circumpolar Permafrost Region. Global Biogeochemical Cycles, 23(2): GB2023:1-GB2023:11. https://doi.org/10.1029/2008gb003327
Tian, W., Wang, H. M., Xiang, X., et al., 2019. Structural Variations of Bacterial Community Driven by Sphagnum Microhabitat Differentiation in a Subalpine Peatland. Frontiers in Microbiology, 10: 1661. https://doi.org/10.3389/fmicb.2019.01661
Trosvik, P., de Muinck, E. J., 2015. Ecology of Bacteria in the Human Gastrointestinal Tract: Identification of Keystone and Foundation Taxa. Microbiome, 3: 44. https://doi.org/10.1186/s40168-015-0107-4
Turetsky, M. R., Bond-Lamberty, B., Euskirchen, E., et al., 2012. The Resilience and Functional Role of Moss in Boreal and Arctic Ecosystems. The New Phytologist, 196(1): 49–67. https://doi.org/10.1111/j.1469-8137.2012.04254.x
van Breemen, N., 1995. How Sphagnum Bogs down other Plants. Trends in Ecology & Evolution, 10(7): 270–275. https://doi.org/10.1016/0169-5347(95)90007-1
Vorob’ev, A. V., de Boer, W., Folman, L. B., et al., 2009. Methylovirgula Ligni Gen. Nov., Sp. Nov., an Obligately Acidophilic, Facultatively Methylotrophic Bacterium with a Highly Divergent mxaF Gene. International Journal of Systematic and Evolutionary Microbiology, 59(10): 2538–2545. https://doi.org/10.1099/ijs.0.010074-0
Wang, Y. Q., Sen, B., He, Y. D., et al., 2018. Spatiotemporal Distribution and Assemblages of Planktonic Fungi in the Coastal Waters of the Bohai Sea. Frontiers in Microbiology, 9: 584. https://doi.org/10.3389/fmicb.2018.00584
Xiang, X., Wang, H. M., Gong, L. F., et al., 2014. Vertical Variations and Associated Ecological Function of Bacterial Communities from Sphagnum to Underlying Sediments in Dajiuhu Peatland. Science China Earth Sciences, 57(5): 1013–1020. https://doi.org/10.1007/s11430-013-4752-9
Xiang, X., Wang, R. C., Wang, H. M., et al., 2017. Distribution of Bathyarchaeota Communities across Different Terrestrial Settings and Their Potential Ecological Functions. Scientific Reports, 7: 45028. https://doi.org/10.1038/srep45028
Xu, Y., 2018. The Diversity and Spacial Distribution of Microbial Community Related To Nitrogen Cycle in the Shennongjia Dajiuhu: [Dissertation]. China University of Geosciences, Wuhan
Xu, Y., Wang, H. M., Xiang, X., et al., 2019. Vertical Variation of Nitrogen Fixers and Ammonia Oxidizers along a Sediment Profile in the Dajiuhu Peatland, Central China. Journal of Earth Science, 30(2): 397–406. https://doi.org/10.1007/s12583-018-0982-2
Yan, Q. Y., Li, J. J., Yu, Y. H., et al., 2016. Environmental Filtering Decreases with Fish Development for the Assembly of Gut Microbiota. Environmental Microbiology, 18(12): 4739–4754. https://doi.org/10.1111/1462-2920.13365
Yu, E. M., Xie, J., Wang, J. L., et al., 2016. Surface-Attached and Suspended Bacterial Community Structure as Affected by C/N Ratios: Relationship between Bacteria and Fish Production. World Journal of Microbiology and Biotechnology, 32(7): 116. https://doi.org/10.1007/s11274-016-2065-9
Zhang, P., Xie, X. J., Li, Q. H., et al., 2022. Microbial Community Structure and Its Response to Environment in Mangrove Sediments of Dongzhai Port. Earth Science, 47(3): 1122–1135. https://doi.org/10.3799/dqkx.2022.025 (in Chinese with English Abstract)
Acknowledgments
The Project was jointly supported by National Natural Science Foundation of China (No. 41572325) and China University of Geosciences (Wuhan) (Nos. CUGCJ1703 and CUGQY1922). The authors would like to thank Weihua Ding, Yong Duan and Ziqi Zhang for their assistance in sample collection. The authors would also like to acknowledge the Bureau of Dajiuhu National Wetland Park for their assistance in authorizing this research and providing access to the Dajiuhu Peatland. The final publication is available at Springer via https://doi.org/10.1007/s12583-020-1391-x.
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Composition and function of bacterial communities of bryophytes and their underlying sediments in the Dajiuhu Peatland, central China
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Xiang, X., Wang, H., Tian, W. et al. Composition and Function of Bacterial Communities of Bryophytes and Their Underlying Sediments in the Dajiuhu Peatland, Central China. J. Earth Sci. 34, 133–144 (2023). https://doi.org/10.1007/s12583-020-1391-x
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DOI: https://doi.org/10.1007/s12583-020-1391-x