Skip to main content
SpringerLink
Log in

Characterizing sediment bacterial community and identifying the biological indicators in a seawater-freshwater transition zone during the wet and dry seasons

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

Abstract

Seawater intrusion has a detrimental effect on agriculture, industry, and human health. One question of particular interest is how the microbial community responds to and reflects seawater intrusion with seasonal variation. The current study explored the seasonal changes in bacterial community composition and interaction in the vicinity of Pearl River Estuary in dry season (January) and wet season (September). Results indicated that the salinity of sediment samples obtained in dry season was higher than that in wet season. The salt stress induced a declined alpha diversity but resulted in a loosely connected and unstable biotic interaction network in the bacterial communities. Random forest prediction and redundancy analysis of bacterial community indicated that salinity substantially affected the bacterial communities. Multiple lines of evidence, including the enrichment of bacterial taxa in the high-salinity location, microbe-microbe interactions, environment-microbe interactions, and machine learning approach, demonstrated that the families Moraxellaceae and Planococcaceae were the keystone taxa and were resistant to salt stress, which suggested that both of them can be used as potential biological indicators of monitoring and controlling seawater intrusion in coastal zone areas.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

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

Similar content being viewed by others

Data availability

All data related to this publication are made available from the corresponding author on reasonable request.

References

  • Agler MT, Ruhe J, Kroll S, Morhenn C, Kim ST, Weigel D, Kemen EM (2016) Microbial hub taxa link host and abiotic factors to plant microbiome variation. PLoS Biol 14:e1002352

    Article  CAS  Google Scholar 

  • Ahmed A, Ghosh PK, Hasan M, Rahman A (2020) Surface and groundwater quality assessment and identification of hydrochemical characteristics of a south-western coastal area of Bangladesh. Environ Monit Assess 192:258

    Article  CAS  Google Scholar 

  • Ardon M, Morse J, Colman B, Bernhardt E (2013): Drought-induced saltwater incursion leads to increased wetland nitrogen export. Glob Change Biol 19

  • Arora S, Patel PN, Vanza MJ, Rao GG (2014) Isolation and characterization of endophytic bacteria colonizing halophyte and other salt tolerant plant species from coastal Gujarat. Afr J Microbiol Res 8:1779–1788

    Article  Google Scholar 

  • Atashgahi S, Sánchez-Andrea I, Heipieper HJ, van der Meer JR, Stams AJM, Smidt H (2018) Prospects for harnessing biocide resistance for bioremediation and detoxification. Science 360:743

    Article  CAS  Google Scholar 

  • Azevedo JS, Correia A, Henriques I (2013) Molecular analysis of the diversity of genus Psychrobacter present within a temperate estuary. FEMS Microbiol Ecol 84:451–460

    Article  CAS  Google Scholar 

  • Bamforth CW, Quayle JR (1978) Aerobic and anaerobic growth of Paracoccus denitrificans on methanol. Arch Microbiol 119:91–97

    Article  CAS  Google Scholar 

  • Banerjee S, Schlaeppi K, van der Heijden MGA (2018) Keystone taxa as drivers of microbiome structure and functioning. Nat Rev Microbiol 16:567–576

    Article  CAS  Google Scholar 

  • Benidire L, El Khalloufi F, Oufdou K, Barakat M, Tulumello J, Ortet P, Heulin T, Achouak W (2020) Phytobeneficial bacteria improve saline stress tolerance in Vicia faba and modulate microbial interaction network. Sci Total Environ 729:139020

    Article  CAS  Google Scholar 

  • Bjørkevoll I, Olsen RL, Skjerdal OT (2003) Origin and spoilage potential of the microbiota dominating genus Psychrobacter in sterile rehydrated salt-cured and dried salt-cured cod (Gadus morhua). Int J Food Microbiol 84:175–187

    Article  Google Scholar 

  • Bolyen E et al (2019) Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nat Biotechnol 37:852–857

    Article  CAS  Google Scholar 

  • Callahan BJ, McMurdie PJ, Rosen MJ, Han AW, Johnson AJ, Holmes SP (2016) DADA2: High-resolution sample inference from Illumina amplicon data. Nat Methods 13:581–583

    Article  CAS  Google Scholar 

  • Cao Y, Zhang B, Zhu Z, Song X, Cai Q, Chen B, Dong G, Ye X (2020) Microbial eco-physiological strategies for salinity-mediated crude oil biodegradation. Sci Total Environ 727:138723

    Article  CAS  Google Scholar 

  • Chaudhuri S, Ale S (2013) Temporal evolution of depth-stratified groundwater salinity in municipal wells in the major aquifers in Texas, USA. Sci Total Environ 472C:370–380

    Google Scholar 

  • Chen L, Hu BX, Dai H, Zhang X, Xia CA, Zhang J (2019) Characterizing microbial diversity and community composition of groundwater in a salt-freshwater transition zone. Sci Total Environ 678:574–584

    Article  CAS  Google Scholar 

  • Chen L, Zhang J, Dai H, Hu BX, Tong J, Gui D, Zhang X, Xia C (2020) Comparison of the groundwater microbial community in a salt-freshwater mixing zone during the dry and wet seasons. J Environ Manage 271:110969

    Article  CAS  Google Scholar 

  • Cordero OX, Datta MS (2016) Microbial interactions and community assembly at microscales. Curr Opin Microbiol 31:227–234

    Article  Google Scholar 

  • Costall AR, Harris BD, Teo B, Schaa R, Wagner FM, Pigois JP (2020) Groundwater throughflow and seawater intrusion in high quality coastal aquifers. Sci Rep 10:9866

    Article  CAS  Google Scholar 

  • Cotecchia V, Grassi D, Polemio M (2005): Carbonate aquifers in Apulia and seawater intrusion. Giornale Geol Appl

  • Coyte K, Schluter J, Foster K (2015) The ecology of the microbiome: networks, competition, and stability. Science 350:663–666

    Article  CAS  Google Scholar 

  • Cui J, Sun T, Chen L, Zhang W (2020) Engineering salt tolerance of photosynthetic cyanobacteria for seawater utilization. Biotechnol Adv 43:107578

    Article  CAS  Google Scholar 

  • Dai X, Wang Y-N, Wang B-J, Liu S-J, Zhou Y-G (2005) Planomicrobium chinense sp. nov., isolated from coastal sediment, and transfer of Planococcus psychrophilus and Planococcus alkanoclasticus to Planomicrobium as Planomicrobium psychrophilum comb. nov. and Planomicrobium alkanoclasticum comb. nov. Int J Syst Evol Micr 55:699–702

    Article  CAS  Google Scholar 

  • Dam THT, Amjath-Babu TS, Zander P, Müller K (2019) Paddy in saline water: analysing variety-specific effects of saline water intrusion on the technical efficiency of rice production in Vietnam. Outlook Agr 48:237–245

    Article  Google Scholar 

  • Dias LM, Folador ARC, Oliveira AM, Ramos RTJ, Silva A, Baraúna RA (2018) Genomic architecture of the two cold-adapted genera Exiguobacterium and Psychrobacter: evidence of functional reduction in the Exiguobacterium antarcticum B7 genome. Genome Biol Evol 10:731–741

    Article  CAS  Google Scholar 

  • Dunne JA, Williams RJ, Martinez ND (2002) Network structure and biodiversity loss in food webs: robustness increases with connectance. Ecol Lett 5:558–567

    Article  Google Scholar 

  • Ferchichi H, Ben Hamouda M, Farhat B, Ben Mammou A (2018): Assessment of groundwater salinity using GIS and multivariate statistics in a coastal Mediterranean aquifer. Int J Environ Sci Te 15

  • Gan L, Li X, Tian Y, Peng B (2020) Genomic insights into the salt tolerance and cold adaptation of Planococcus halotolerans SCU63(T). Arch Microbiol 202:2841–2847

    Article  CAS  Google Scholar 

  • Han X, Qu Y, Dong Y, Chen D, Liang D, Liu J, Zhang J, Ren N, Feng Y (2021) Simultaneous electricity generation and eutrophic water treatment utilizing iron coagulation cell with nitrification and denitrification biocathodes. Sci Total Environ 782:146436

    Article  CAS  Google Scholar 

  • Heiss J, Michael H (2014): Saltwater-freshwater mixing dynamics in a sandy beach aquifer over tidal, spring-neap, and seasonal cycles. Water Resour Res 50

  • Hoque M, Scheelbeek P, Vineis P, Khan A, Ahmed KM, Butler A (2016) Drinking water vulnerability to climate change and alternatives for adaptation in coastal South and South East Asia. Clim Change 136

  • Huang X, Lin J, Ye X, Wang G (2015) Molecular characterization of a thermophilic and salt- and alkaline-tolerant xylanase from Planococcus sp. SL4, a strain isolated from the sediment of a Soda Lake. J Microbiol Biotechnol 25:662–671

    Article  CAS  Google Scholar 

  • Jack G, Dawn F, Swift P, Newbold L, Oliver A, Smyth T, Somerfield P, Huse S, Joint I (2009) The seasonal structure of microbial communities in the Western English Channel. Environ Microbiol 11:3132–3139

    Article  CAS  Google Scholar 

  • Jung J-H, Joe M-H, Kim D-H, Park H, Choi J-i, Lim S (2018) Complete genome sequence of Planococcus sp. PAMC21323 isolated from Antarctica and its metabolic potential to detoxify pollutants. Stand Genomic Sci 13: 31

  • Kazakis N, A P, Vargemezis G, G S, Pliakas F-K (2016): Seawater intrusion mapping using electrical resistivity tomography and hydrochemical data. An application in the coastal area of eastern Thermaikos Gulf, Greece. Sci Total Environ 543:373–387

  • Kelly SA, Moody TS, Gilmore BF (2019) Biocatalysis in seawater: investigating a halotolerant ω-transaminase capable of converting furfural in a seawater reaction medium. Eng Life Sci 19:721–725

    Article  CAS  Google Scholar 

  • Khat HV, Dang NH, Yabe M (2018) Impact of salinity intrusion on rice productivity in the Vietnamese Mekong Delta. J Fac Agr Kyushu U 63:143–148

    Google Scholar 

  • Klassen J, Allen DM (2017) Assessing the risk of saltwater intrusion in coastal aquifers. J Hydrol 551:730–745

    Article  Google Scholar 

  • Kumar V, Paranjpe J, Gosavi S, Kulkarni R, Gosavi R (2015) A comparison of three drug combinations for sedation during middle ear surgeries under local Anesthesia: a multicentric randomized double blind study. J Krishna Instit Med Sci Univ 4:32–40

    CAS  Google Scholar 

  • Li (2020): Saltwater intrusion in the Pearl River Estuary (China): variation characteristics and cause analysis. J Coastal Res 36

  • Li Y, Li Q, Chen S (2021a): Diazotroph Paenibacillus triticisoli BJ-18 drives the variation in bacterial, diazotrophic and fungal communities in the rhizosphere and root/shoot endosphere of maize. Int J Mol Sci 22

  • Li Y, Lin H, Gao P, Yang N, Xu R, Sun X, Li B, Xu F, Wang X, Song B, Sun W (2021) Variation in the diazotrophic community in a vertical soil profile contaminated with antimony and arsenic. Environ Pollut 291:118248

    Article  CAS  Google Scholar 

  • Li Y, Wang M, Chen S (2021c): Application of N2-fixing Paenibacillus triticisoli BJ-18 changes the compositions and functions of the bacterial, diazotrophic, and fungal microbiomes in the rhizosphere and root/shoot endosphere of wheat under field conditions. Biol Fert Soils

  • Li Y, Zhang M, Xu R, Lin H, Sun X, Xu F, Gao P, Kong T, Xiao E, Yang N, Sun W (2021) Arsenic and antimony co-contamination influences on soil microbial community composition and functions: relevance to arsenic resistance and carbon, nitrogen, and sulfur cycling. Environ Int 153:106522

    Article  CAS  Google Scholar 

  • Lomstein BA, Langerhuus AT, D’Hondt S, Jørgensen BB, Spivack AJ (2012) Endospore abundance, microbial growth and necromass turnover in deep sub-seafloor sediment. Nature 484:101–104

    Article  CAS  Google Scholar 

  • Lozupone CA, Knight R (2007) Global patterns in bacterial diversity. Proc Natl Acad Sci U S A 104:11436–11440

    Article  CAS  Google Scholar 

  • Maliszewska-Kordybach B, Klimkowicz-Pawlas A, Smreczak B (2007) Ecotoxic effect of phenanthrene on nitrifying bacteria in soils of different properties. J Environ Qual 36:1635–1645

    Article  CAS  Google Scholar 

  • Neubauer S, Craft C (2009): Global change and tidal freshwater wetlands: scenarios and impacts. In: A B, DF W , AH B (Editors), Tidal Freshwater Wetlands, pp. 253–266

  • Newman MEJ (2006) Modularity and community structure in networks. P Natl Acad Sci USA 103:8577

    Article  CAS  Google Scholar 

  • Oren A (2002) Diversity of halophilic microorganisms: environments, phylogeny, physiology, and applications. J Ind Microbiol Biot 28:56–63

    Article  CAS  Google Scholar 

  • Patel V, Munot H, Shouche Y, Madamwar D (2014) Response of bacterial community structure to seasonal fluctuation and anthropogenic pollution on coastal water of Alang-Sosiya ship breaking yard, Bhavnagar, India. Bioresource Technol 161C:362–370

    Article  CAS  Google Scholar 

  • Peng J, Wegner CE, Liesack W (2017) Short-term exposure of paddy soil microbial communities to salt stress triggers different transcriptional responses of key taxonomic groups. Front Microbiol 8:400

    Google Scholar 

  • Petelet E, Négrel P, Aunay B, Ladouche B, Bailly-Comte V, Guerrot C, Flehoc C, Pezard P, Lofi J, Dörfliger N (2016) Coastal groundwater salinization: focus on the vertical variability in a multi-layered aquifer through a multi-isotope fingerprinting (Roussillon Basin, France). Sci Total Environ 566–567:398–415

    Article  CAS  Google Scholar 

  • Romano I, Giordano A, Lama L, Nicolaus B, Gambacorta A (2003) Planococcus rifietensis sp. nov, isolated from algal mat collected from a sulfurous spring in Campania (Italy). Syst Appl Microbiol 26:357–366

    Article  CAS  Google Scholar 

  • Sand M, de Berardinis V, Mingote A, Santos H, Göttig S, Müller V, Averhoff B (2011) Salt adaptation in Acinetobacter baylyi: identification and characterization of a secondary glycine betaine transporter. Arch Microbiol 193:723–730

    Article  CAS  Google Scholar 

  • Sand M, Mingote AI, Santos H, Müller V, Averhoff B (2013) Mannitol, a compatible solute synthesized by Acinetobacter baylyi in a two-step pathway including a salt-induced and salt-dependent mannitol-1-phosphate dehydrogenase. Environ Microbiol 15:2187–2197

    Article  CAS  Google Scholar 

  • Scholz A, Stahl J, de Berardinis V, Müller V, Averhoff B (2016) Osmotic stress response in Acinetobacter baylyi: identification of a glycine-betaine biosynthesis pathway and regulation of osmoadaptive choline uptake and glycine-betaine synthesis through a choline-responsive BetI repressor. Environ Microbiol Rep 8:316–322

    Article  CAS  Google Scholar 

  • Shammi M, Rahman MM, Bondad SE, Bodrud-Doza M (2019): Impacts of salinity intrusion in community health: a review of experiences on drinking water sodium from coastal areas of Bangladesh. Healthcare 7

  • Sherif M, Kacimov A, Javadi A, Ebraheem AA (2012) Modeling groundwater flow and seawater intrusion in the coastal aquifer of Wadi Ham, UAE. Water Resour Manag 26:751–774

    Article  Google Scholar 

  • Sinsabaugh RL, Hill BH, Follstad Shah JJ (2010) Erratum: Ecoenzymatic stoichiometry of microbial organic nutrient acquisition in soil and sediment. Nature 468:122–122

    Article  CAS  Google Scholar 

  • Slomp CP, Van Cappellen P (2004) Nutrient inputs to the coastal ocean through submarine groundwater discharge: controls and potential impact. J Hydrol 295:64–86

    Article  CAS  Google Scholar 

  • Stuyfzand PJ, Maas K, Kappelhof J, Kooiman JW (2004) Pumping brackish groundwater to prepare drinking water and keep salinized wells fresh, 18th Salt Water Intrusion Meeting. Cartagena, Spain

    Google Scholar 

  • Sylus KJ, Ramesh H (2015) The study of sea water intrusion in coastal aquifer by electrical conductivity and total dissolved solid method in Gurpur and Netravathi river basin. Aquatic Proc 4:57–64

    Article  Google Scholar 

  • Tiwari AK, Pisciotta A, De Maio M (2019) Evaluation of groundwater salinization and pollution level on Favignana Island, Italy. Environ Pollut 249:969–981

    Article  CAS  Google Scholar 

  • Unno T, Kim J, Kim Y, Nguyen SG, Guevarra RB, Kim GP, Lee J-H, Sadowsky MJ (2015) Influence of seawater intrusion on microbial communities in groundwater. Sci Total Environ 532:337–343

    Article  CAS  Google Scholar 

  • van der Heijden MG, Hartmann M (2016) Networking in the plant microbiome. PLoS Biol 14:e1002378

    Article  CAS  Google Scholar 

  • Wang K, Zou L, Lu X, Mou X (2018) Organic carbon source and salinity shape sediment bacterial composition in two China marginal seas and their major tributaries. Sci Total Environ 633:1510–1517

    Article  CAS  Google Scholar 

  • Wang Q, Xie Z, Li F (2015) Using ensemble models to identify and apportion heavy metal pollution sources in agricultural soils on a local scale. Environ Pollut 206:227–235

    Article  CAS  Google Scholar 

  • Wang X, Yang T, Lin B, Tang Y (2017) Effects of salinity on the performance, microbial community, and functional proteins in an aerobic granular sludge system. Chemosphere 184:1241–1249

    Article  CAS  Google Scholar 

  • Wang Y, Jiao JJ (2012) Origin of groundwater salinity and hydrogeochemical processes in the confined Quaternary aquifer of the Pearl River Delta, China. J Hydrol 438–439:112–124

    Article  CAS  Google Scholar 

  • Wang Y, Hou Y, Nie P, Wang Y, Ren X, Wei Q, Wang Q (2019): A novel cold-adapted and salt-tolerant RNase R from Antarctic sea-ice bacterium Psychrobacter sp. ANT206. Molecules 24

  • Wang Y, Wang Q, Hou Y (2020): A new cold-adapted and salt-tolerant glutathione reductase from Antarctic psychrophilic bacterium Psychrobacter sp. and its resistance to oxidation. Int J Mol Sci 21

  • Xu Z, Woodhouse JN, Te SH, Yew-Hoong Gin K, He Y, Xu C, Chen L (2018) Seasonal variation in the bacterial community composition of a large estuarine reservoir and response to cyanobacterial proliferation. Chemosphere 202:576–585

    Article  CAS  Google Scholar 

  • Xun W, Huang T, Li W, Ren Y, Xiong W, Ran W, Li D, Shen Q, Zhang R (2017) Alteration of soil bacterial interaction networks driven by different long-term fertilization management practices in the red soil of South China

  • Yong L, Han L, Gao P, Yang N, Xu R, Sun X, Li B, Xu F, Wang X, Song B, Sun W (2021): Synergistic impacts of arsenic and antimony co-contamination on diazotrophic communities. Microb Ecol

  • Zeng X, Wu J, Wang D, Zhu X (2016) Assessing the pollution risk of a groundwater source field at western Laizhou Bay under seawater intrusion. Environ Res 148:586–594

    Article  CAS  Google Scholar 

  • Zghibi A, Mirchi A, Zouhri L, Taupin JD, Chekirbane A, Tarhouni J (2019) Implications of groundwater development and seawater intrusion for sustainability of a Mediterranean coastal aquifer in Tunisia. Environ Monit Assess 191:696

    Article  CAS  Google Scholar 

  • Zhang W, Chen X, Tan H, Zhang Y, Cao J (2015) Geochemical and isotopic data for restricting seawater intrusion and groundwater circulation in a series of typical volcanic islands in the South China Sea. Mar Pollut Bull 93

  • Zheng T, Deng Y, Wang Y, Jiang H, O’Loughlin EJ, Flynn TM, Gan Y, Ma T (2019) Seasonal microbial variation accounts for arsenic dynamics in shallow alluvial aquifer systems. J Hazard Mater 367:109–119

    Article  CAS  Google Scholar 

  • Zhou W, Luo L, Xu H, Wang D (2012) Saltwater intrusion in the Pearl River Estuary during winter. Aquat Ecosyst Health 15:70–80

    Article  Google Scholar 

Download references

Acknowledgements

This work was supported by the China Postdoctoral Science Foundation (Grant No. 2021M690745), the Science and Technology Planning Project of Guangzhou (Grant Nos. 202002020072 and 201904010366), the National Natural Science Foundation of China (Grant No. 41771301), GDAS’ Project of Science and Technology Development (Grant Nos. 2021GDASYL-20210103048, 2020GDASYL-20200102015, 2019GDASYL-0102002-4, and 2019GDASYL-0102002-1), Guangdong Basic and Applied Basic Research Foundation (Grant Nos. 2021A1515011374 and 2021A1515011461), the National Natural Science Foundation of China (Grant No. U20A20109), the Science and Technology Planning Project of Guangdong Province (Grant No. 2019B110210003), and Guangdong Introducing Innovative and Entrepreneurial Talents (Grant No. 2017GC010570).

Author information

Author notes

  1. Yongbin Li, Duanyi Huang and Weimin Sun contributed equally to this work

Authors and Affiliations

  1. National-Regional Joint Engineering Research Center for Soil Pollution Control and Remediation in South China, Guangdong Key Laboratory of Integrated Agro-Environmental Pollution Control and Management, Institute of Eco-Environmental and Soil Sciences, Guangdong Academy of Sciences, Tianhe District, 808 Tianyuan Road, Guangzhou, 510650, Guangdong, China

    Yongbin Li, Duanyi Huang, Weimin Sun, Xiaoxu Sun, Geng Yan, Wenlong Gao & Hanzhi Lin

Authors
  1. Yongbin Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Duanyi Huang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Weimin Sun
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Xiaoxu Sun
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Geng Yan
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Wenlong Gao
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Hanzhi Lin
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Yongbin Li wrote the original draft, and Hanzhi Lin conceptualized and designed the study. Yongbin Li, Duanyi Huang, Weimin Sun, and Xiaoxu Sun performed the experiment and data analysis. Geng Yan and Wenlong Gao commented on and revised the manuscript. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Hanzhi Lin.

Ethics declarations

Ethical approval

Not applicable.

Consent to participate

Not applicable.

Consent to publish

Not applicable.

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 356 kb)

Supplementary file2 (XLSX 14 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Li, Y., Huang, D., Sun, W. et al. Characterizing sediment bacterial community and identifying the biological indicators in a seawater-freshwater transition zone during the wet and dry seasons. Environ Sci Pollut Res 29, 41219–41230 (2022). https://doi.org/10.1007/s11356-021-18053-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-021-18053-6

Keywords

Search

Navigation