SpringerLink
Log in

Rapid shifts in pond sediment microbiota in response to high ambient temperature in a water–sediment microcosm

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

Unlike the extensive research on the response of soil microorganisms to high ambient temperature (HTA), the response of sediment microorganisms to HTA remains unclear. Understanding the response of sediment microorganisms to HTA is important to forecast their impacts on ecosystems and climate warming under projected climate change scenarios. Against the background of climate warming and frequent high ambient temperatures in summer, we conducted a laboratory incubation experiment to clarify the unique assembly characteristics of pond sediment bacterial communities at different temperatures (4, 10, 15, 25, 30 and 35 °C). The results showed that the structure and function of the microbial community in pond sediments at 35 °C were different from those under other temperatures; the microbial community structure at 35 °C had the most large modules and an average module size. Temperature and dissolved oxygen influenced the microbial community network modularity. The CO2 emission rates of pond sediments at 35 °C were significantly higher than those at other temperatures. At 35 °C, heterogeneous selection was the most important assembly process. Additionally, warming altered the microbial network structure and ecosystem functioning but not the microbial diversity or community composition, which may be related to horizontal gene transfer. Revealing the rapid response of pond sediment microorganisms to HTA is important for identifying their role in nutrient cycling and assessing the ecological impacts of climate warming and high ambient temperatures on inland water sediments.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price includes VAT (Germany)

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

Data availability

The data supporting the findings of this study are available within the article and/or its supplementary materials.

References

  • Ai H, Qiu Y, He Q, He Y, Yang C, Kang L, Luo H, Li W, Mao Y, Hu M, Li H (2019) Turn the potential greenhouse gases into biomass in harmful algal blooms waters: a microcosm study. Sci Total Environ 655:520–528

    CAS  Google Scholar 

  • Banerjee S, Schlaeppi K, Heijden, M.G.A.v.d., (2018) Keystone taxa as drivers of microbiome structure and functioning. Nat Rev Microbiol 16:567–576

    CAS  Google Scholar 

  • Bérard A, Bouchet T, Sévenier G, Pablo AL, Gros R (2011) Resilience of soil microbial communities impacted by severe drought and high temperature in the context of Mediterranean heat waves. Eur J Soil Biol 47(6):333–342

    Google Scholar 

  • Chen IC, Hegde U, Chang CH, Yang SS (2008) Methane and carbon dioxide emissions from closed landfill in Taiwan. Chemosphere 70(8):1484–1491

    CAS  Google Scholar 

  • Chen ZJ, Xu G, Ding CY, Zheng BH, Chen Y, Han H, Li YY, Shi JW, Hu LQ (2020) Illumina MiSeq sequencing and network analysis the distribution and co-occurrence of bacterioplankton in Danjiangkou Reservoir, China. Arch Microbiol 202(4):859–873

    CAS  Google Scholar 

  • Colby GA, Ruuskanen MO, St Pierre KA, St Louis VL, Poulain AJ, Aris-Brosou S (2020) Warming climate is reducing the diversity of dominant microbes in the largest high arctic lake. Front Microbiol 11:561194

    Google Scholar 

  • Comer-Warner SA, Romeijn P, Gooddy DC, Ullah S, Kettridge N (2018) Thermal sensitivity of CO2 and CH4 emissions varies with streambed sediment properties. Nat Commun 9(1):2803

    Google Scholar 

  • Cram JA, **a LC, Needham DM, Sachdeva R, Sun F, Fuhrman JA (2015) Cross-depth analysis of marine bacterial networks suggests downward propagation of temporal changes. ISME J 9(12):2573–2586

    Google Scholar 

  • Dacal M, Garcia-Palacios P, Asensio S, Cano-Diaz C, Gozalo B, Ochoa V, Maestre FT (2020) Contrasting mechanisms underlie short- and longer-term soil respiration responses to experimental warming in a dryland ecosystem. Glob Chang Biol 26(9):5254–5266

    Google Scholar 

  • de Vries FT, Griffiths RI, Bailey M, Craig H, Girlanda M, Gweon HS, Hallin S, Kaisermann A, Keith AM, Kretzschmar M, Lemanceau P, Lumini E, Mason KE, Oliver A, Ostle N, Prosser JI, Thion C, Thomson B, Bardgett RD (2018) Soil bacterial networks are less stable under drought than fungal networks. Nat Commun 9(1):3033

    Google Scholar 

  • Downing JA, Cole JJ, Middelburg JJ, Striegl RG, Duarte CM, Kortelainen P, Prairie YT, Laube KA (2008) Sediment organic carbon burial in agriculturally eutrophic impoundments over the last century. Global Biogeochem. Cycles 20(1):GB1018

    Google Scholar 

  • Faust K, Sathirapongsasuti JF, Izard J, Segata N, Gevers D, Raes J, Huttenhower C (2012) Microbial co-occurrence relationships in the human microbiome. PLoS Comput Biol 8(7):e1002606

    CAS  Google Scholar 

  • Feng W, Liang J, Hale LE, Jung CG (2017) Enhanced decomposition of stable soil organic carbon and microbial catabolic potentials by long-term field warming. Global Change Biol 23(11):4765–4776

    Google Scholar 

  • Fuchs A, Klier J, Pinto F, Selmeczy GB, Szabó B, Padisák J, Jürgens K, Casper P (2017) Effects of artificial thermocline deepening on sedimentation rates and microbial processes in the sediment. Hydrobiologia 799(1):65–81

    CAS  Google Scholar 

  • Gonzalez JM, Portillo MC, Piñeiro-Vidal M (2014) Latitude-dependent underestimation of microbial extracellular enzyme activity in soils. Int J Environ Sci Technol (tehran) 12(7):2427–2434

    Google Scholar 

  • Gudasz C, Bastviken D, Steger K, Premke K, Sobek S, Tranvik LJ (2010) Temperature-controlled organic carbon mineralization in lake sediments. Nature 466(7305):478–481

    CAS  Google Scholar 

  • Guidi L, Chaffron S, Bittner L, Eveillard D, Larhlimi A, Roux S, Darzi Y, Audic S, Berline L, Brum JR, Coelho LP, Espinoza JCI, Malviya S, Sunagawa S, Dimier C, Kandels-Lewis S, Picheral M, Poulain J, Searson S, Stemmann L, Not F, Hingamp P, Speich S, Follows M, Karp-Boss L, Boss E, Ogata H, Pesant S, Weissenbach J, Wincker P, Acinas SG, Bork P, de Vargas C, Iudicone D, Sullivan MB, Raes J, Karsenti E, Bowler C, Gorsky G (2016) Plankton networks driving carbon export in the oligotrophic ocean. Nature 532(7600):465–470

    CAS  Google Scholar 

  • Guo X, Feng J, Shi Z, Zhou X, Yuan M, Tao X, Hale L, Yuan T, Wang J, Qin Y, Zhou A, Fu Y, Wu L, He Z, Van Nostrand JD, Ning D, Liu X, Luo Y, Tiedje JM, Yang Y, Zhou J (2018) Climate warming leads to divergent succession of grassland microbial communities. Nat Clim Change 8(9):813–818

    Google Scholar 

  • Guo X, Zhou X, Hale L, Yuan M, Ning D, Feng J, Shi Z, Li Z, Feng B, Gao Q, Wu L, Shi W, Zhou A, Fu Y, Wu L, He Z, Van Nostrand JD, Qiu G, Liu X, Luo Y, Tiedje JM, Yang Y, Zhou J (2019) Climate warming accelerates temporal scaling of grassland soil microbial biodiversity. Nat Ecol Evol 3(4):612–619

    Google Scholar 

  • Haggerty R, Argerich A and Martí E (2008) Development of a “smart” tracer for the assessment of microbiological activity and sediment-water interaction in natural waters: The resazurin-resorufin system. Water Resour Res 44(4):W00D01

  • He Q, Wang S, Hou W, Feng K, Li F, Hai W, Zhang Y, Sun Y, Deng Y (2021) Temperature and microbial interactions drive the deterministic assembly processes in sediments of hot springs. Sci Total Environ 772:145465

    CAS  Google Scholar 

  • Herren C, McMahon K (2017) Cohesion: a method for quantifying the connectivity of microbial communities. ISME J 11:2426–2438

    Google Scholar 

  • Holgerson MA, Raymond PA (2016) Large contribution to inland water CO2 and CH4 emissions from very small ponds. Nat Geosci 9(3):222–226

    CAS  Google Scholar 

  • Huang M, Chai L, Jiang D, Zhang M, Jia W, Huang Y and Zhou J (2021) Dissolved organic matter (DOM) quality drives biogeographic patterns of soil bacterial communities and their association networks in semi-arid regions. FEMS Microbiol Ecol 97(7):fiab083

  • Jiao S, Chen W, Wei G, Kivlin S (2021) Linking phylogenetic niche conservatism to soil archaeal biogeography, community assembly and species coexistence. Global Ecol Biogeogr 30(7):1488–1501

    Google Scholar 

  • Lin Q, De Vrieze J, Li C, Li J, Li J, Yao M, Hedenec P, Li H, Li T, Rui J, Frouz J, Li X (2017) Temperature regulates deterministic processes and the succession of microbial interactions in anaerobic digestion process. Water Res 123:134–143

    CAS  Google Scholar 

  • Liu M, Han X, Tong J, Zhu H and Bai X (2020) Mutual environmental drivers of the community composition, functional attributes and co-occurrence patterns of bacterioplankton in the composite aquatic ecosystem of Taihu watershed in China. FEMS Microbiol Ecol 96(8):fiaa137

  • Lu WW, Yao X, Ren H, Deng H, Yao M, Zhang B (2020) Characterizing the interactions between sediment dissolved organic matter and zinc using multispectroscopic techniques. Environ Pollut 261:113644

    CAS  Google Scholar 

  • Marotta H, Pinho L, Gudasz C, Bastviken D, Tranvik LJ, Enrich-Prast A (2014) Greenhouse gas production in low-latitude lake sediments responds strongly to warming. Nat Clim Change 4(6):467–470

    CAS  Google Scholar 

  • Masson-Delmotte P, Zhai HO, Pörtner D, Roberts J and Skea PR (2018). IPCC, 2018: Global Warming of 1.5°C.An IPCC Special Report on the impacts of global warming of 1.5°C above pre-industrial levels and related global greenhouse gas emission pathways, in the context of strengthening the global response to the threat of climate change, sustainable development, and efforts to eradicate poverty. In Press

  • Mendonca R, Muller RA, Clow D, Verpoorter C, Raymond P, Tranvik LJ, Sobek S (2017) Organic carbon burial in global lakes and reservoirs. Nat Commun 8(1):1694

    Google Scholar 

  • Mitavskiy B, Rowe J, Cannings C (2008) Preliminary theoretical analysis of a local search algorithm to optimize network communication subject to preserving the total number of links. IEEE Congress Evol Comput (IEEE World Congress Comput Intell) 2008:1484–1491

    Google Scholar 

  • Ning D, Yuan M, Wu L, Zhang Y, Guo X, Zhou X, Yang Y, Arkin AP, Firestone MK, Zhou J (2020) A quantitative framework reveals ecological drivers of grassland microbial community assembly in response to warming. Nat Commun 11(1):4717

    CAS  Google Scholar 

  • Pachauri RK and Meyer LA (2014) IPCC, 2014: Climate change 2014: synthesis report. Contribution of working groups i, ii and iii to the fifth assessment report of the intergovernmental panel on climate change, p. 151

  • Qian Z, Jian S, Nunan N, Maestre FT, Tedersoo L, He J, Wei H, Tan X, Shen W (2017) Altered precipitation seasonality impacts the dominant fungal but rare bacterial taxa in subtropical forest soils. Biol Fert Soils 53:231–245

    Google Scholar 

  • R Core Team (2020) R: a language and environment for statistical computing (R foundation for statistical computing, 2022)

  • Rein I, Gessler A, Premke K, Keitel C, Ulrich A, Kayler ZE (2016) Forest understory plant and soil microbial response to an experimentally induced drought and heat-pulse event: the importance of maintaining the continuum. Global Change Biol 22(8):2861–2874

    Google Scholar 

  • Sepulveda-Jauregui A, Hoyos-Santillan J, Martinez-Cruz K, Walter Anthony KM, Casper P, Belmonte-Izquierdo Y, Thalasso F (2018) Eutrophication exacerbates the impact of climate warming on lake methane emission. Sci Total Environ 636:411–419

    CAS  Google Scholar 

  • She Z, Pan X, Wang J, Shao R, Wang G, Wang S and Yue Z (2021) Vertical environmental gradient drives prokaryotic microbial community assembly and species coexistence in a stratified acid mine drainage lake. Water Res 206:117739

  • Shi A, Zhou X, Yao S and Zhang B (2020) Effects of intensities and cycles of heating on mineralization of organic matter and microbial community composition of a Mollisol under different land use types. Geoderma 357:140109

  • Stegen JC, Lin X, Fredrickson JK, Chen X, Kennedy DW, Murray CJ, Rockhold ML, Konopka A (2013) Quantifying community assembly processes and identifying features that impose them. ISME J 7(11):2069–2079

    Google Scholar 

  • **ao N, Zhou A, Kempher ML, Zhou J (2022) Disentangling direct from indirect relationships in association networks. Proc Ind Nat Sci Acad 119(2):e2109995119

    CAS  Google Scholar 

  • Xu H, Li H, Tang Z, Liu Y, Li G, He Q (2020) Underestimated methane production triggered by phytoplankton succession in river-reservoir systems: evidence from a microcosm study. Water Res 185:116233

    CAS  Google Scholar 

  • Xu M, Li X, Kuyper TW, Xu M, Li X, Zhang J (2021) High microbial diversity stabilizes the responses of soil organic carbon decomposition to warming in the subsoil on the Tibetan Plateau. Global Change Biol 27(10):2061–2075

    CAS  Google Scholar 

  • Yan D, Xu H, Lan J, Yang M, Wang F, Hou W, Zhou K, An Z (2020) Warming favors subtropical lake cyanobacterial biomass increasing. Sci Total Environ 726:138606

    CAS  Google Scholar 

  • Yuan MM, Guo X, Wu L, Zhang Y (2021) Climate warming enhances microbial network complexity and stability. Nat Clim Change 11(4):343–348

    Google Scholar 

  • Zhang L, Yin W, Wang C, Zhang A, Zhang H, Zhang T, Ju F (2021) Untangling microbiota diversity and assembly patterns in the world’s largest water diversion canal. Water Res 204:117617

    CAS  Google Scholar 

  • Zhao LL, Zhu GW, Chen YF, Li W, Zhu MY, Yao X, Cai LL (2011) Thermal stratification and its influence factors in a large-sized and shallow Lake Taihu. Adv Water Sci (China) 22(6):844–850

    Google Scholar 

  • Zhou J, Deng Y, Luo F, He Z, Yang Y (2011) Phylogenetic molecular ecological network of soil microbial communities in response to elevated CO2. MBio 2(4):e00122-00111

    Google Scholar 

  • Zhou L, Zhou Y, Tang X, Zhang Y, Jang KS, Szekely AJ, Jeppesen E (2021a) Resource aromaticity affects bacterial community successions in response to different sources of dissolved organic matter. Water Res 190:116776

    CAS  Google Scholar 

  • Zhou L, Zhou Y, Tang X, Zhang Y, Jeppesen E (2021b) Biodegradable dissolved organic carbon shapes bacterial community structures and co-occurrence patterns in large eutrophic Lake Taihu. J Environ Sci 107:205–217

    CAS  Google Scholar 

Download references

Funding

We gratefully thank the Major Science and Technology Program for Water Pollution Control and Treatment of China (No.2017ZX07206), the National Natural Science Foundation of China (No. 41977322) and the National Natural Science Foundation of China (No. 41907335) for their financial support of this study.

Author information

Authors and Affiliations

  1. State Key Laboratory of Environmental Criteria and Risk Assessment, National Engineering Laboratory for Lake Pollution Control and Ecological Restoration, State Environmental Protection Key Laboratory for Lake Pollution Control, Chinese Research Academy of Environmental Sciences, Bei**g, 100012, China

    Weiwei Lü, Haoyu Ren, Wanchang Ding, He Li & **a Jiang

  2. College of Water Sciences, Bei**g Normal University, Bei**g, 100875, China

    Weiwei Lü & Haoyu Ren

  3. School of Environment and Planning, University of Liaocheng, Liaocheng, 252000, China

    **n Yao

Authors
  1. Weiwei Lü
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Haoyu Ren
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Wanchang Ding
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. He Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. **n Yao
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. **a Jiang
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Weiwei Lü: Data curation, formal analysis, methodology, writing—original draft, writing—review and editing. **a Jiang: Co-supervising, data curation, writing—review and editing. Haoyu Ren: Investigation, formal analysis, visualization, software. Wanchang Ding, He Li: writing—review and editing.

Corresponding author

Correspondence to **a Jiang.

Ethics declarations

Ethics approval

Not applicable.

Consent to participate

Not applicable.

Consent for publication

All authors agree to publication.

Competing interests

The authors declare no competing interests.

Additional information

Responsible Editor: Robert Duran

Publisher's note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 3226 KB)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Lü, W., Ren, H., Ding, W. et al. Rapid shifts in pond sediment microbiota in response to high ambient temperature in a water–sediment microcosm. Environ Sci Pollut Res 30, 74358–74371 (2023). https://doi.org/10.1007/s11356-023-26823-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-023-26823-7

Keywords

Search

Navigation