Abstract
Aims
Microbial-driven biogeochemical cycles of phosphorus (P) in wetlands subjected to global climate warming result in a downstream eutrophication risk. However, how warming influences P associated with microbial shifts in wetland soils is largely unknown.
Methods
A custom-built, novel microcosm that simulated climate warming was established under ambient temperature and elevated warming conditions (+ 3 °C). 31P nuclear magnetic resonance (31P–NMR) technology was used to characterize different P forms and high-throughput sequencing of 16S rRNA gene was used to identify microbial community and functional potentials in wetland soils varied with nutrition status.
Results
Soil P forms were dominated by orthophosphate. The dynamic changes of different P forms in response to warming were mainly observed in high nutrition wetlands. The relative abundance of orthophosphate and polyphosphate (inorganic) significantly (p < 0.05) decreased, which was accompanied with increased phosphonate (organic) under warming. Consistently, soil microbial community shifts were also found in high nutrition wetlands, especially in fall with significantly (p < 0.05) increased relative abundance of Alphaproteobacteria and Betaproteobacteria and decreased Clostridia under warming. The microbial functions related to catabolism, the transport, degradation and release of P were enriched under warming. Changed microbial community may have altered the overall functional potentials which were responsible for P dynamics.
Conclusions
Soil microbial community shifts in response to experimental warming were season-based. Microbial changes and P shifts from high nutrition wetlands were more sensitive to warming. The changed microbial community under warming conditions may trigger the loss of orthophosphate through the altered functional potentials. These findings aid to better understand microbial-driven biogeochemical cycles of P in wetland soils under future climate changes.
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References
Ahlgren J, Tranvik L, Gogoll A et al (2005) Sediment depth attenuation of biogenic phosphorus compounds measured by 31P-NMR. Environ Sci Technol 39:867–872. https://doi.org/10.1021/es049590h
Andrews JA, Matamala R, Westover KM et al (2000) Temperature effects on the diversity of soil heterotrophs and the 13C of soil-respired CO2. Soil Biol Biochem 32:699–706. https://doi.org/10.1016/S0038-0717(99)00206-0
Caporaso JG et al (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336. https://doi.org/10.1038/nmeth.f.303
Chen M, Ye TR, Krumholz LR et al (2014) Temperature and cyanobacterial bloom biomass influence phosphorous cycling in eutrophic lake sediments. PLoS One 9:e93130. https://doi.org/10.1371/journal.pone.0093130
Chernov TI, Tkhakakhova AK, Ivanova EA et al (2015) Seasonal dynamics of the microbiome of chernozems of the long-term agrochemical experiment in Kamennaya steppe. Eurasian Soil Sci 48:1349–1353. https://doi.org/10.1134/S1064229315120054
Cole JR et al (2009) The ribosomal database project: improved alignments and new tools for rRNA analysis. Nucleic Acids Res 37:141–145. https://doi.org/10.1093/nar/gkn879
DeAngelis KM, Pold G, Topçuoğlu BD et al (2015) Long-term forest soil warming alters microbial communities in temperate forest soils. Front Microbiol 6:104. https://doi.org/10.3389/fmicb.2015.00104
Doolette AL, Smernik RJ, Dougherty WJ (2009) Spiking improved solution phosphorus-31 nuclear magnetic resonance identification of soil phosphorus compounds. Soil Sci Soc Am J 73:919–927. https://doi.org/10.2136/sssaj2008.0192
Falkowski PG, Fenchel T, Delong EF (2008) The microbial engines that drive Earth's biogeochemical cycles. Science 320:1034–1039. https://doi.org/10.1126/science.1153213
Feuchtmayr H, Moran R, Hatton K et al (2009) Global warming and eutrophication: effects on water chemistry and autotrophic communities in experimental hypertrophic shallow lake mesocosms. J Appl Ecol 46:713–723. https://doi.org/10.1111/j.1365-2664.2009.01644.x
Frey SD, Drijber R, Smith H, Melillo J (2008) Microbial biomass, functional capacity, and community structure after 12 years of soil warming. Soil Biol Biochem 40:2904–2907. https://doi.org/10.1016/j.soilbio.2008.07.020
García-López AM, Avilés M, Delgado A (2016) Effect of various microorganisms on phosphorus uptake from insoluble ca phosphates by cucumber plants. J Plant Nutr Soil Sci 179:454–465. https://doi.org/10.1002/jpln.201500024
Giles CD, Lee LG, Cade-Menun BJ, Hill JE et al (2015) Characterization of organic phosphorus form and bioavailability in lake sediments using 31P nuclear magnetic resonance and enzymatic hydrolysis. J Environ Qual 44:882–894. https://doi.org/10.2134/jeq2014.06.0273
Gyaneshwar P, Kumar GN, Parekh LJ et al (2002) Role of soil microorganisms in improving P nutrition of plants. Plant Soil 245:83–93
Hammer Ø, Harper DAT, Ryan PD (2001) PAST: paleontological statistics software package for education and data analysis. Palaeontol Electron 4:9
Hui D, Mayes MA, Wang G (2013) Kinetic parameters of phosphatase: a quantitative synthesis. Soil Biol Biochem 65:105–113. https://doi.org/10.1016/j.soilbio.2013.05.017
Hupfer M, Lewandowski J (2008) Oxygen controls the phosphorus release from Lake sediments-a long-lasting paradigm in limnology. Int Rev Hydrobiol 93:415–432. https://doi.org/10.1002/iroh.200711054
Issartel JP et al (1992) The ATP synthase (F0-F1) complex in oxidative phosphorylation. Experientia 48:351–362
Jiao S et al (2016) Bacterial communities in oil contaminated soils: biogeography and co-occurrence patterns. Soil Biol Biochem 98:64–73. https://doi.org/10.1016/j.soilbio.2016.04.005
Jin H, Sun OJ, Liu J (2010) Changes in soil microbial biomass and community structure with addition of contrasting types of plant litter in a semiarid grassland ecosystem. J Plant Ecol 3:209–217. https://doi.org/10.1093/jpe/rtq001
Jin Y, Liang X, He M, Liu Y et al (2016) Manure biochar influence upon soil properties, phosphorus distribution and phosphatase activities: a microcosm incubation study. Chemosphere 142:128–135. https://doi.org/10.1016/j.chemosphere.2015.07.015
Kuffner M, Hai B, Rattei T et al (2012) Effects of season and experimental warming on the bacterial community in a temperate mountain forest soil assessed by 16S rRNA gene pyrosequencing. FEMS Microbiol Ecol 82:551–562. https://doi.org/10.1111/j.1574-6941.2012.01420.x
Kumar M, Tomar RS, Lade H, Paul D (2016) Methylotrophic bacteria in sustainable agriculture. World J Microbiol Biotechnol 32:1–9. https://doi.org/10.1007/s11274-016-2074-8
Langille MG et al (2013) Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nat Biotechnol 31:814–821. https://doi.org/10.1038/nbt.2676
Lindstrom SM, White JR (2011) Reducing phosphorus flux from organic soils in surface flow treatment wetlands. Chemosphere 85:625–629. https://doi.org/10.1016/j.chemosphere.2011.06.109
McDonald D et al (2012) An improved Greengenes taxonomy with explicit ranks for ecological and evolutionary analyses of bacteria and archaea. ISME J 6:610–618. https://doi.org/10.1038/ismej.2011.139
Mohammadi K (2012) Phosphorus solubilizing bacteria: occurrence, mechanisms and their role in crop production. Res Envrion 2:80–85. https://doi.org/10.5923/j.re.20120201.10
Rinnan R, Rousk J, Yergeau E et al (2009) Temperature adaptation of soil bacterial communities along an Antarctic climate gradient: predicting responses to climate warming. Glob Chang Biol 15:2615–2625. https://doi.org/10.1111/j.1365-2486.2009.01959.x
Ristova PP, Bienhold C, Wenzhöfer F et al (2017) Temporal and spatial variations of bacterial and faunal communities associated with Deep-Sea wood falls. PLoS One 12:e0169906. https://doi.org/10.1371/journal.pone.0169906
Saarenheimo J, Tiirola MA, Rissanen AJ (2015) Functional gene pyrosequencing reveals core proteobacterial denitrifiers in boreal lakes. Front Microbiol 6:674. https://doi.org/10.3389/fmicb.2015.00674
Scheffran J, Battaglini A (2011) Climate and conflicts: the security risks of global warming. Reg Environ Chang 11:27–39. https://doi.org/10.1007/s10113-010-0175-8
Schindlbacher A, Rodler A, Kuffner M et al (2011) Experimental warming effects on the microbial community of a temperate mountain forest soil. Soil Biol Biochem 43:1417–1425. https://doi.org/10.1016/j.soilbio.2011.03.005
Segata N, Izard J, Waldron L et al (2011) Metagenomic biomarker discovery and explanation. Genome Biol 12:R60. https://doi.org/10.1186/gb-2011-12-6-r60
Shen J, Yuan L, Zhang J et al (2011) Phosphorus dynamics: from soil to plant. Plant Physiol 156:997–1005. https://doi.org/10.1104/pp.111.175232
Solomon S, et al (ed). 2007. Climate change 2007: the physical science basis. Contribution of Working Group I to the Fourth Assessment Report of the IPCC. Cambridge University Press, Cambridge
Sondergaard M, Jensen JP, Jeppesen E (2003) Role of sediment and internal loading of phosphorus in shallow lakes. Hydrobiologia 506:135–145. https://doi.org/10.1023/B:HYDR.0000008611.12704.dd
Tapia-Torres Y, Rodríguez-Torres MD, Elser JJ et al (2016) How to live with phosphorus scarcity in soil and sediment: lessons from bacteria. Appl Environ Microbiol 82:00. https://doi.org/10.1128/AEM.00160-16
Turner BL, Cade-Menun BJ, Condron LM, Newman S (2005) Extraction of soil organic phosphorus. Talanta 66:294–306. https://doi.org/10.1016/j.talanta.2004.11.012
Wakai S, Masanari M, Ikeda T et al (2013) Oxidative phosphorylation in a thermophilic, facultative chemoautotroph, Hydrogenophilus thermoluteolus, living prevalently in geothermal niches. Environ Microbiol Rep 5:235–242. https://doi.org/10.1111/1758-2229.12005
Wang H, Holden J, Spera K et al (2013) Phosphorus fluxes at the sediment-water interface in subtropical wetlands subjected to experimental warming: a microcosm study. Chemosphere 90:1794–1804. https://doi.org/10.1016/j.chemosphere.2012.08.044
Wang H, Li HY, Zhang ZJ et al (2014) Linking stoichiometric homeostasis of microorganisms with soil phosphorus dynamics in wetlands subjected to microcosm warming. PLoS One 9:e85575. https://doi.org/10.1371/journal.pone.0085575
Wang H, Li HY, Ping F et al (2016a) Microbial acclimation triggered loss of soil carbon fractions in subtropical wetlands subjected to experimental warming in a laboratory study. Plant Soil 406:101–116. https://doi.org/10.1007/s11104-016-2868-3
Wang J, Xue C, Song Y et al (2016b) Wheat and rice growth stages and fertilization regimes alter soil bacterial community structure, but not diversity. Front Microbiol 7. https://doi.org/10.3389/fmicb.2016.01207
Wei Y, Wei Z, Cao Z et al (2016) A regulating method for the distribution of phosphorus fractions based on environmental parameters related to the key phosphate-solubilizing bacteria during composting. Bioresour Technol 211:610–617. https://doi.org/10.1016/j.biortech.2016.03.141
Young EO, Ross DS, Cade-Menun BJ (2013) Phosphorus speciation in riparian soils: a 31P nuclear magnetic resonance spectroscopy and enzyme hydrolysis study. Soil Sci Soc Am J 77:1636–1647. https://doi.org/10.2136/sssaj2012.0313
Yu H, Luedeling E, Xu J (2010) Winter and spring warming result in delayed spring phenology on the Tibetan Plateau. Proc Natl Acad Sci 107:22151–22156
Yuan H, Pan W, Shen J et al (2015) Species and environmental geochemistry characteristics of organic phosphorus in sediments of riverine wetland measured by 31P-NMR spectroscopy. Geochem Int 53:1141–1149. https://doi.org/10.1134/S0016702915120058
Zhang ZJ, Wang ZD, Holden J et al (2012) The release of phosphorus from sediment into water in subtropical wetlands: a warming microcosm experiment. Hydrol Process 26:15–26. https://doi.org/10.1002/hyp.8105
Zhang ZJ, Wang H, Zhou JZ et al (2015) Redox potential and microbial functional gene diversity in wetland sediments under simulated warming conditions: implications for phosphorus mobilization. Hydrobiologia 743:221–235. https://doi.org/10.1007/s10750-014-2039-6
Zhang W et al (2016) Composition of phosphorus in wetland soils determined by SMT and solution 31P-NMR analyses. Environ Sci Pollut Res 23:9046–9053. https://doi.org/10.1007/s11356-015-5974-5
Acknowledgements
This work was supported by the National Natural Science Foundation of China (41373073, 31500409).
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Wang, H., Teng, C., Li, H. et al. Microbial community shifts trigger loss of orthophosphate in wetland soils subjected to experimental warming. Plant Soil 424, 351–365 (2018). https://doi.org/10.1007/s11104-017-3538-9
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DOI: https://doi.org/10.1007/s11104-017-3538-9