Abstract
The microbial community plays an important role in the biogeochemical cycle in coastal groundwater ecosystems. However, the composition and controlling factors of the microbial community in coastal closed groundwater systems (CCGSs) with high salinity have rarely been studied. Here, we investigated and analyzed the hydrochemical characteristics and microbial community composition of seven brine samples with high total dissolved solid (TDS) values ranging from 74.5 to 132.3 g/L within and across three coastal saltworks (Yangkou, Hanting, and Changyi) in southern Laizhou Bay (SLB). The bacterial diversity was independent of salinity. Compared with those of low-salinity groundwater, the diversity of the microbial community in brine was lower, but the richness was slightly higher. There was a significant correlation between the microbial community diversity and groundwater sources, which indicated that the microbial communities were affected by groundwater sources. A comparison of the microbial community compositions of the three saltworks showed that the Hanting and Changyi saltworks had similar microbial communities due to their similar sampling depths. In addition, the main force shaping the differences in the microbial communities in both coastal open groundwater systems (COGSs) and CCGSs was identified as the hydraulic connection with the seawater controlled by hydrogeological conditions formed throughout geological history. This study can help to elucidate the biogeochemical processes in coastal aquifers.
Similar content being viewed by others
Data availability
Not applicable.
References
Adyasari D, Hassenrück C, Oehler T et al (2019) Microbial community structure associated with submarine groundwater discharge in northern Java (Indonesia). Sci Total Environ 689:590–601. https://doi.org/10.1016/j.scitotenv.2019.06.193
Alcalá FJ, Custodio E (2008) Using the Cl/Br ratio as a tracer to identify the origin of salinity in aquifers in Spain and Portugal. J Hydrol 359:189–207. https://doi.org/10.1016/j.jhydrol.2008.06.028
Andronov EE, Petrova SN, Pinaev AG et al (2012) Analysis of the structure of microbial community in soils with different degrees of salinization using T-RFLP and real-time PCR techniques. Eurasian Soil Sci 45:147–156. https://doi.org/10.1134/S1064229312020044
Anitua E, Tejero R, Pacha-Olivenza MÁ et al (2018) Balancing microbial and mammalian cell functions on calcium ion-modified implant surfaces. J Biomed Mater Res - Part B Appl Biomater 106:421–432. https://doi.org/10.1002/jbm.b.33860
Benizri E, Dedourge O, Dibattista-Leboeuf C et al (2002) Effect of maize rhizodeposits on soil microbial community structure. Appl Soil Ecol 21:261–265. https://doi.org/10.1016/S0929-1393(02)00094-X
Bozau E, Sattler CD, Van Berk W (2015) Hydrochemical Classification of Deep Formation Waters. Appl Geochemistry 52:23–30. https://doi.org/10.1016/j.apgeochem.2014.10.018
Bray JR, Curtis JT (1957) An ordination of the upland forest communities of southern Wisconsin. Ecol Monogr 27:325–349. https://doi.org/10.2307/1942268
Bush T, Diao M, Allen RJ et al (2017) Oxic-anoxic regime shifts mediated by feedbacks between biogeochemical processes and microbial community dynamics. Nat Commun 8:1–9. https://doi.org/10.1038/s41467-017-00912-x
Canfora L, Bacci G, Pinzari F, et al (2014) Salinity and bacterial diversity: to what extent does the concentration of salt affect the bacterial community in a saline soil? PLoS One 9:. https://doi.org/10.1371/journal.pone.0106662
Cao Q, Wang H, Chen X et al (2017) Composition and distribution of microbial communities in natural river wetlands and corresponding constructed wetlands. Ecol Eng 98:40–48. https://doi.org/10.1016/j.ecoleng.2016.10.063
Caporaso JG, Kuczynski J, Stombaugh J et al (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336
Chang Y, Hu BX, Xu Z et al (2018) Numerical simulation of seawater intrusion to coastal aquifers and brine water/freshwater interaction in south coast of Laizhou Bay, China. J Contam Hydrol 215:1–10. https://doi.org/10.1016/j.jconhyd.2018.06.002
Chao A, Bunge J (2002) Estimating the number of species in a stochastic abundance model. Biometrics 58:531–539. https://doi.org/10.1111/j.0006-341X.2002.00531.x
Chen L, Hu BX, Dai H et al (2019) Characterizing microbial diversity and community composition of groundwater in a salt-freshwater transition zone. Sci Total Environ 678:574–584. https://doi.org/10.1016/j.scitotenv.2019.05.017
Chen L, Zhang J, Dai H et al (2020) Comparison of the groundwater microbial community in a salt-freshwater mixing zone during the dry and wet seasons. J Environ Manage 271:110969. https://doi.org/10.1016/j.jenvman.2020.110969
Craig H (1961) Standard for reporting concentrations of deuterium and oxygen-18 in natural waters. Science (80- ) 133:1833–1834. https://doi.org/10.1126/science.133.3467.1833
Dakin RA, Farvolden RN, Cherry JA, Fritz P (1983) Origin of dissolved solids in groundwaters of Mayne Island, British Columbia, Canada. J Hydrol 63:233–270. https://doi.org/10.1016/0022-1694(83)90044-6
Dong J, Zhao D, Zhang C et al (2020) Factors controlling organic carbon distributions in a riverine wetland. Environ Sci Pollut Res 27:34529–34540. https://doi.org/10.1007/s11356-020-09685-1
Drever J (1997) The geochemistry of natural water: surface and groundwater environments, 3rd edn. Prentice Hall, New Jersey, pp 329–332
Du Y, Ma T, Chen L et al (2015) Applied geochemistry genesis of salinized groundwater in Quaternary aquifer system of coastal plain. Laizhou Bay, China: Geochemical Evidences, Especially from Bromine Stable Isotope 59:155–165. https://doi.org/10.1016/j.apgeochem.2015.04.017
Faith DP (1992) Conservation evaluation and phylogenetic diversity. Biol Conserv 61:1–10. https://doi.org/10.1016/0006-3207(92)91201-3
Fiedler CJ, Schönher C, Proksch P et al (2018) Assessment of microbial community dynamics in river bank filtrate using high-throughput sequencing and flow cytometry. Front Microbiol 9:1–15. https://doi.org/10.3389/fmicb.2018.02887
Gao M, Guo F, Hou G, et al (2018) The evolution of sedimentary environment since late Pleistocene in Laizhou Bay, Bohai Sea. Geol China 45:59–68. https://doi.org/10.12029/gc20180106
Gao Y, Wang C, Zhang W et al (2017) Vertical and horizontal assemblage patterns of bacterial communities in a eutrophic river receiving domestic wastewater in southeast China. Environ Pollut 230:469–478. https://doi.org/10.1016/j.envpol.2017.06.081
Gonfiantini R (1978) Standards for stable isotope measurements in natural compounds. Nature 271:534–536. https://doi.org/10.1038/271534a0
Guo L, Wang G, Sheng Y et al (2019) Groundwater microbial communities and their connection to hydrochemical environment in Golmud. Northwest China Sci Total Environ 695:133848. https://doi.org/10.1016/j.scitotenv.2019.133848
Guo L, Wang G, Sheng Y et al (2020) Science of the total environment temperature governs the distribution of hot spring microbial community in three hydrothermal fields, Eastern Tibetan Plateau Geothermal Belt. Western China Sci Total Environ 720:137574. https://doi.org/10.1016/j.scitotenv.2020.137574
Han D, Cao G, Currell MJ et al (2020) Groundwater salinization and flushing during glacial-interglacial cycles: insights from aquitard porewater tracer profiles in the North China Plain. Water Resour Res 56:1–23. https://doi.org/10.1029/2020WR027879
Han DM, Song XF, Currell MJ et al (2014) Chemical and isotopic constraints on evolution of groundwater salinization in the coastal plain aquifer of Laizhou Bay, China. J Hydrol 508:12–27. https://doi.org/10.1016/j.jhydrol.2013.10.040
Hardie L (1987) Perspectives. Dolomitization: a critical view of some current views. J Sediment Petrol 57:166–183. https://doi.org/10.1306/212F8AD5-2B24-11D7-8648000102C1865D
Herlemann DPR, Labrenz M, Jürgens K et al (2011) Transitions in bacterial communities along the 2000 km salinity gradient of the Baltic Sea. ISME J 5:1571–1579. https://doi.org/10.1038/ismej.2011.41
Hollister EB, Engledow AS, Hammett AJM et al (2010) Shifts in microbial community structure along an ecological gradient of hypersaline soils and sediments. ISME J 4:829–838. https://doi.org/10.1038/ismej.2010.3
Houben G, Post VEA (2017) Les premières descriptions sur le terrain d’intrusion d’eau salée induite par pompage et d’upconing. Hydrogeol J 25:243–247. https://doi.org/10.1007/s10040-016-1476-x
Hu SY, Xiao CL, Liang XJ, Cao YQ (2020) Influence of water-rock interaction on the ph and heavy metals content of groundwater during in-situ oil shale exploitation. Oil Shale 37:104–118. https://doi.org/10.3176/oil.2020.2.02
Karczewski K, Riss HW, Meyer EI (2017) Comparison of DNA-fingerprinting (T-RFLP) and high-throughput sequencing (HTS) to assess the diversity and composition of microbial communities in groundwater ecosystems. Limnologica 67:45–53. https://doi.org/10.1016/j.limno.2017.10.001
Kirchman DL, Dittel AI, Malmstrom RR, Cottrell MT (2005) Biogeography of major bacterial groups in the Delaware Estuary. Limnol Oceanogr 50:1697–1706. https://doi.org/10.4319/lo.2005.50.5.1697
Klindworth A, Pruesse E, Schweer T et al (2013) Evaluation of general 16S ribosomal RNA gene PCR primers for classical and next-generation sequencing-based diversity studies. Nucleic Acids Res 41:e1–e1. https://doi.org/10.1093/nar/gks808
Korbel KL, Hose GC (2011) A tiered framework for assessing groundwater ecosystem health. Hydrobiologia 661:329–349. https://doi.org/10.1007/s10750-010-0541-z
Kozich JJ, Westcott SL, Baxter NT et al (2013) Development of a dual-index sequencing strategy and curation pipeline for analyzing amplicon sequence data on the miseq illumina sequencing platform. Appl Environ Microbiol 79:5112–5120. https://doi.org/10.1128/AEM.01043-13
Lee S, Currell M, Cendón DI (2016) Marine water from mid-Holocene sea level highstand trapped in a coastal aquifer: evidence from groundwater isotopes, and environmental significance. Sci Total Environ 544:995–1007. https://doi.org/10.1016/j.scitotenv.2015.12.014
Lee JH, Unno T, Ha K (2018) Vertical and horizontal distribution of bacterial communities in alluvial groundwater of the Nakdong River bank. Geomicrobiol J 35:74–80. https://doi.org/10.1080/01490451.2017.1321066
Liao H, Yu K, Duan Y et al (2019) Profiling microbial communities in a watershed undergoing intensive anthropogenic activities. Sci Total Environ 647:1137–1147. https://doi.org/10.1016/j.scitotenv.2018.08.103
Lin W, Zhang W, Paterson GA et al (2020) Expanding magnetic organelle biogenesis in the domain Bacteria. Microbiome 8:1–13. https://doi.org/10.1186/s40168-020-00931-9
Liu J, Yang H, Zhao M, Zhang XH (2014a) Spatial distribution patterns of benthic microbial communities along the Pearl Estuary, China. Syst Appl Microbiol 37:578–589. https://doi.org/10.1016/j.syapm.2014.10.005
Liu K, Jiao JJ, Gu JD (2014b) Investigation on bacterial community and diversity in the multilayer aquifer-aquitard system of the Pearl River Delta, China. Ecotoxicology 23:2041–2052. https://doi.org/10.1007/s10646-014-1311-x
Liu S, Tang Z, Gao M, Hou G (2017) Evolutionary process of saline-water intrusion in Holocene and Late Pleistocene groundwater in southern Laizhou Bay. Sci Total Environ 607–608:586–599. https://doi.org/10.1016/j.scitotenv.2017.06.262
Lozupone CA, Knight R (2007) Global patterns in bacterial diversity. Proc Natl Acad Sci U S A 104:11436–11440. https://doi.org/10.1073/pnas.0611525104
Lutterodt G, Miyittah MK, Addy B, Ansa EDO, Takase M (2021) Groundwater pollution assessment in a coastal aquifer in Cape Coast. Ghana Heliyon 7:e06751. https://doi.org/10.1016/j.heliyon.2021.e06751
Ma Q, Li H, Wang X, Wang C (2015) Estimation of seawater – groundwater exchange rate: case study in a tidal fl at with a large-scale seepage face ( Laizhou Bay , China ). 265–275. https://doi.org/10.1007/s10040-014-1196-z
McFeters GA, Stuart DG (1972) Survival of coliform bacteria in natural waters: field and laboratory studies with membrane-filter chambers. Appl Microbiol 24:805–811. https://doi.org/10.1128/aem.24.5.805-811.1972
Michael HA, Post VEA, Wilson AM, Werner AD (2017) Science, society, and the coastal groundwater squeeze. Water Resour Res 53:2610–2617. https://doi.org/10.1002/2017WR020851
Nguyen TT, Kawamura A, Tong TN et al (2015) Clustering spatio-seasonal hydrogeochemical data using self-organizing maps for groundwater quality assessment in the Red River Delta. Vietnam J Hydrol 522:661–673. https://doi.org/10.1016/j.jhydrol.2015.01.023
Pang Z, Kong Y, Li J, Tian J (2017) An isotopic geoindicator in the hydrological cycle. Procedia Earth Planet Sci 17:534–537. https://doi.org/10.1016/j.proeps.2016.12.135
Park S-J, Andrei A-Ş, Bulzu P-A et al (2020) Expanded diversity and metabolic versatility of marine nitrite-oxidizing bacteria revealed by cultivation- and genomics-based approaches. Appl Environ Microbiol 86:e01667-e1720. https://doi.org/10.1128/AEM.01667-20
Priestley SC, Meredith KT, Treble PC et al (2020) A 35 ka record of groundwater recharge in south-west Australia using stable water isotopes. Sci Total Environ 717:135105. https://doi.org/10.1016/j.scitotenv.2019.135105
Qi H, Ma C, He Z et al (2019) Lithium and its isotopes as tracers of groundwater salinization: a study in the southern coastal plain of Laizhou Bay, China. Sci Total Environ 650:878–890. https://doi.org/10.1016/j.scitotenv.2018.09.122
Rath KM, Fierer N, Murphy DV, Rousk J (2019) Linking bacterial community composition to soil salinity along environmental gradients. ISME J 13:836–846. https://doi.org/10.1038/s41396-018-0313-8
Reed HE, Martiny JBH (2013) Microbial composition affects the functioning of estuarine sediments. ISME J 7:868–879. https://doi.org/10.1038/ismej.2012.154
Roeßler M, Sewald X, Müller V (2003) Chloride dependence of growth in bacteria. FEMS Microbiol Lett 225:161–165. https://doi.org/10.1016/S0378-1097(03)00509-3
Salama R, Otto C, Fitzpatrick R (1999) Contributions of groundwater conditions to soil and water salinization. Hydrogeol J 7:46–64. https://doi.org/10.1007/s100400050179
Sang S, Dai H, Hu BX et al (2019) The study of hydrogeochemical environments and microbial communities along a groundwater salinity gradient in the Pearl River Delta, China. Water (switzerland) 11:1–18. https://doi.org/10.3390/w11040804
Sang S, Zhang X, Dai H et al (2018) Diversity and predictive metabolic pathways of the prokaryotic microbial community along a groundwater salinity gradient of the Pearl River Delta. China Sci Rep 8:17317. https://doi.org/10.1038/s41598-018-35350-2
Sawyer AH, Michael HA, Schroth AW (2016) From soil to sea: the role of groundwater in coastal critical zone processes. Wiley Interdiscip Rev Water 3:706–726. https://doi.org/10.1002/wat2.1157
Sirisena KA, Daughney CJ, Moreau M, Sim DA, Lee CK, Cary SC, Ryan KG, Chambers GK (2018) Bacterial bioclusters relate to hydrochemistry in New Zealand groundwater. FEMS Microbiol Ecol. 94. https://doi.org/10.1093/femsec/fiy170
Sonthiphand P, Ruangroengkulrith S, Mhuantong W, Charoensawan V, Chotpantarat S, Boonkaewwan S (2019) Metagenomic insights into microbial diversity in a groundwater basin impacted by a variety of anthropogenic activities. Environ Sci Pollut Res 26:26765–26781. https://doi.org/10.1007/s11356-019-05905-5
Staley C, Unno T, Gould TJ et al (2013) Application of Illumina next-generation sequencing to characterize the bacterial community of the Upper Mississippi River. J Appl Microbiol 115:1147–1158. https://doi.org/10.1111/jam.12323
Strickland MS, Lauber C, Fierer N, Bradford MA (2009) Testing the functional significance of microbial community composition. Ecology 90:441–451. https://doi.org/10.1890/08-0296.1
Tian Bozau E, Sattler CD, van Berk W (2015) Hydrogeochemical classification of deep formation waters. Appl Geochemistry 52:23–30. https://doi.org/10.1016/j.apgeochem.2014.10.018
Tian QQ, Liang L, Zhu MJ (2015) Enhanced biohydrogen production from sugarcane bagasse by Clostridium thermocellum supplemented with CaCO3. Bioresour Technol 197:422–428. https://doi.org/10.1016/j.biortech.2015.08.111
Tian R, Ning D, He Z et al (2020) Small and mighty: adaptation of superphylum Patescibacteria to groundwater environment drives their genome simplicity. Microbiome 8:1–15. https://doi.org/10.1186/s40168-020-00825-w
TJR (2006) Report of ‘‘Study of real-time monitoring and warning on sea-salt water intrusion in Laizhou Bay—a case study of Changyi-Liutuan profile’’. Tianjin Institute of Geology and Mineral Resources, 37–38 (unpublished in Chinese).
Toplin JA, Norris TB, Lehr CR et al (2008) Biogeographic and phylogenetic diversity of thermoacidophilic cyanidiales in Yellowstone National Park, Japan, and New Zealand. Appl Environ Microbiol 74:2822–2833. https://doi.org/10.1128/AEM.02741-07
Unno T, Jang J, Han D et al (2010) Use of barcoded pyrosequencing and shared OTUs to determine sources of fecal bacteria in watersheds. Environ Sci Technol 44:7777–7782. https://doi.org/10.1021/es101500z
Valenzuela-Encinas C, Neria-González I, Alcántara-Hernández RJ et al (2009) Changes in the bacterial populations of the highly alkaline saline soil of the former lake Texcoco (Mexico) following flooding. Extremophiles 13:609–621. https://doi.org/10.1007/s00792-009-0244-4
Wang J, Yang D, Zhang Y et al (2011) Do patterns of bacterial diversity along salinity gradients differ from those observed for macroorganisms? PLoS ONE 6:e27597. https://doi.org/10.1371/journal.pone.0027597
Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naïve Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73:5261–5267. https://doi.org/10.1128/AEM.00062-07
Wen X, Lu J, Wu J et al (2019) Science of the total environment influence of coastal groundwater salinization on the distribution and risks of heavy metals. Sci Total Environ 652:267–277. https://doi.org/10.1016/j.scitotenv.2018.10.250
Wu QL, Zwart G, Schauer M et al (2006) Bacterioplankton community composition along a salinity gradient of sixteen high-mountain lakes located on the Tibetan Plateau, China. Appl Environ Microbiol 72:5478–5485. https://doi.org/10.1128/AEM.00767-06
Xu N, Tan G, Wang H, Gai X (2016) Effect of biochar additions to soil on nitrogen leaching, microbial biomass and bacterial community structure. Eur J Soil Biol 74:1–8. https://doi.org/10.1016/j.ejsobi.2016.02.004
Xu Z, Hu BX, Ye M (2018) Numerical modeling and sensitivity analysis of seawater intrusion in a dual-permeability coastal karst aquifer with conduit networks. Hydrol Earth Syst Sci 22:221–239. https://doi.org/10.5194/hess-22-221-2018
Yang F, Liu S, Jia C et al (2021) Hydrochemical characteristics and functions of groundwater in southern Laizhou Bay based on the multivariate statistical analysis approach. Estuar Coast Shelf Sci 250:107153. https://doi.org/10.1016/j.ecss.2020.107153
Yang F, Wang R, Xu S et al (2016) Hydrogeochemical and stable isotopic characteristics of brine in Laizhou Bay. Geol Rev 62:343–350 (in Chinese)
Yin Z, Luo Q, Wu J et al (2020) Identification of the long-term variations of groundwater and their governing factors based on hydrochemical and isotopic data in a river basin. J Hydrol 592:125604. https://doi.org/10.1016/j.jhydrol.2020.125604
Zhang M, Yu N, Chen L et al (2012) Structure and seasonal dynamics of bacterial communities in three urban rivers in China. Aquat Sci 74:113–120. https://doi.org/10.1007/s00027-011-0201-z
Zhang X, Hu BX, Ren H, Zhang J (2018) Composition and functional diversity of microbial community across a mangrove-inhabited mudflat as revealed by 16S rDNA gene sequences. Sci Total Environ 633:518–528. https://doi.org/10.1016/j.scitotenv.2018.03.158
Zhang X, Qi L, Li W et al (2021) Science of the total environment bacterial community variations with salinity in the saltwater-intruded estuarine aquifer. Sci Total Environ 755:142423. https://doi.org/10.1016/j.scitotenv.2020.142423
Zhao Z, Fu Y, Xu J, Zhang Z, Liu Z, He J (2016) An investigation on high-efficiency profile grinding of directional solidified nickel-based superalloys DZ125 with electroplated CBN wheel. Int J Adv Manuf Technol 83:1–11. https://doi.org/10.1007/s00170-015-7550-z
Zheng T, Deng Y, Wang Y et al (2019) Seasonal microbial variation accounts for arsenic dynamics in shallow alluvial aquifer systems. J Hazard Mater 367:109–119. https://doi.org/10.1016/j.jhazmat.2018.12.087
Zheng Y, Gao M, Liu S, et al (2014) Distribution characteristics of subsurface brine resources on the southern coast of laizhou bay since late pleistocene. Hydrogeol & Eng Geol 41:11–18. https://doi.org/10.16030/j.cnki.issn.1000-3665.2014.05.030
Zhou Y, Kellermann C, Griebler C (2012) Spatio-temporal patterns of microbial communities in a hydrologically dynamic pristine aquifer. FEMS Microbiol Ecol 81:230–242. https://doi.org/10.1111/j.1574-6941.2012.01371.x
Zhu A, Yang Z, Liang Z, et al (2020) Integrating hydrochemical and biological approaches to investigate the surface water and groundwater interactions in the hyporheic zone of the Liuxi River basin, southern China. J Hydrol 583:. https://doi.org/10.1016/j.jhydrol.2020.124622
Funding
This research is financially supported by the National Science Foundation of China (No. 42007166,41977173), the Fundamental Research Funds of Shandong University (Grant No.2019GN057), the Open Research Fund of State Key Laboratory of Estuarine and Coastal Research (Grant No. SKLEC-KF202010), and the Joint Funds of National Nature Science Foundation of China-Shandong Province(U1706219).
Author information
Authors and Affiliations
Contributions
FY: investigation, conceptualization, formal analysis, investigation, writing—original draft; SL: idea, investigation, conceptualization, writing—review and editing; CJ: writing—review and editing; YW: writing—review and editing.
Corresponding authors
Ethics declarations
Ethics approval and consent to participate
This manuscript does not report on or involve the use of any animal or human data or tissue; therefore, it is not applicable for this part.
Consent for publication
This manuscript does not contain any individual person’s data in any form (including any individual details, images, or videos); therefore, it is not applicable for this part.
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.
Highlights
• The diversity and composition of the microbial community in SLB brine were identified.
• Groundwater sources and sampling depths affected the diversity and composition of the groundwater microbial community.
• The hydrogeological conditions of different coastal zone types might be the main factor affecting the composition of bacterial communities.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Yang, F., Liu, S., Jia, C. et al. Identification of groundwater microbial communities and their connection to the hydrochemical environment in southern Laizhou Bay, China. Environ Sci Pollut Res 29, 14263–14278 (2022). https://doi.org/10.1007/s11356-021-16812-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-021-16812-z