Abstract
The aim of this study was to reveal the variation in dissolved organic matter (DOM) components, bacterial community composition, and their co-relationships during groundwater migration. A well-studied shallow eutrophic lake, Lake Taihu, was selected to explore the DOM components and bacterial communities during groundwater replenishment from the lake using three-dimensional fluorescence-parallel factor analysis and high-throughput sequencing, respectively. Six fluorescent components of DOM were identified, including four humic-like components (C1: \({\lambda }_{Ex/Em}=330/400 nm\), C2: \({\lambda }_{Ex/Em}=260, 350/450 nm\), C3: \({\lambda }_{Ex/Em}=270, 380/480 nm\), and C6: \({\lambda }_{Ex/Em}=220/410 nm\)) and two protein-like components (C4: \({\lambda }_{Ex/Em}=230, 280/320 nm\), C5: \({\lambda }_{Ex/Em}=230, 290/340 nm\)). With increasing distance to Lake Taihu, the fluorescence intensity of C1, C3, C4, and C5 decreased within 15 km away from lake shore and then tended to be stable. Thirty-three phyla of bacteria were identified in the aquifer, including Proteobacteria (61.9% of total bacteria), Bacteroidetes (15.0%), Planctomycetes (4.8%), Verrucomicrobia (3.4%), and Actinobacteria (3.3%). The relative abundance of Proteobacteria was significantly positively correlated with the fluorescence intensity of C1–C3, while the relative abundance of Actinobacteria showed the opposite relationship with the fluorescence intensity of C1–C3. The relative abundances of Novosphingobium and Limnohabitans were positively correlated with the fluorescence intensity of C4–C6. Our work suggests that the influence of groundwater replenishment from a eutrophic lake on DOM in the surrounding aquifer may extend to within 15 km from the lake shore. A large amount of DOM inputs (especially humic acid-like components) can induce variation in groundwater bacterial community composition and thus affects the groundwater biogeochemistry.
Similar content being viewed by others
Data availability
The data for this study can be accessed upon request to the corresponding author.
References
APHA (2005) Standard Methods for the Examination of Water and Wastewater. Washington, DC, USA
Aukes PJK, Schiff SL, Robertson WD (2019) Evolution of dissolved organic matter along a septic system plume: evidence of sustained biogeochemical activity in the groundwater zone. J Geophys Res-Biogeosci 124:1389–1400. https://doi.org/10.1029/2018JG004758
Birdwell JE, Engel AS (2010) Characterization of Dissolved organic matter in cave and spring waters using uv-vis absorbance and fluorescence spectroscopy. Org Geochem 41:270–280. https://doi.org/10.1016/j.orggeochem.2009.11.002
Bitton G, Gabriel C (1984) Groundwater pollution microbiology. John Wiley and Sons, New York
Butler RG, Orlob GT, McGauhey PH (1954) Underground movement of bacterial and chemical pollutants. J Am Water Work Assoc 46:97–111. https://doi.org/10.1002/j.1551-8833.1954.tb16148.x
Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Peña AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336. https://doi.org/10.1038/nmeth.f.303
Chakravarhty SS, Pande S, Kapoor A, Nerurkar AS (2011) Comparison of denitrification between Paracoccus sp. and Diaphorobacter sp. Appl Biochem Biotechnol 165:260–269. https://doi.org/10.1007/s12010-011-9248-5
Chang WJ, Sun JL, Pang Y, Zhang SH, Gong LX, Lu JA, Feng B, Xu RC (2020) Effects of different habitats on the bacterial community composition in the water and sediments of Lake Taihu, China. Environ Sci Pollut Res 27:44983–44994. https://doi.org/10.1007/s11356-020-10376-0
Chen ML, Price RM, Yamashita Y, Jaffé R (2010) Comparative study of dissolved organic matter from groundwater and surface water in the Florida coastal everglades using multi-dimensional spectrofluorometry combined with multivariate statistics. Appl Geochem 25:872–880. https://doi.org/10.1016/j.apgeochem.2010.03.005
Chen BF, Huang W, Ma SZ, Feng MH, Liu C, Gu XZ, Chen KN (2018) Characterization of chromophoric dissolved organic matter in the littoral zones of eutrophic lakes Taihu and Hongze during the algal bloom season. Water 10:861. https://doi.org/10.3390/w10070861
Chik AHS, Emelko MB, Anderson WB, O′Sullivan KE, Savio D, Farnleitner AH, Blaschke AP, Schijven JF (2020) Evaluation of groundwater bacterial community composition to inform waterborne pathogen vulnerability assessments. Sci Total Environ 743:140472. https://doi.org/10.1016/j.scitotenv.2020.140472
Corapcioglu MY, Haridas A (1985) Microbial transport in soils and groundwater: a numerical model. Adv Water Resour 8:188–200. https://doi.org/10.1016/0309-1708(85)90063-6
DeSantis TZ, Hugenholtz P, Larsen N, Rojas M, Brodie EL, Keller K, Huber T, Dalevi D, Hu P, Andersen GL (2006) Greengenes, a Chimera-Checked 16S rRNA Gene Database and Workbench Compatible with ARB. Appl Environ Microbiol 72:5069–5072. https://doi.org/10.1128/AEM.03006-05
Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460–2461. https://doi.org/10.1093/bioinformatics/btq461
Goldscheider N, Hunkeler D, Rossi P (2006) Review: microbial biocenoses in pristine aquifers and an assessment of investigative methods. Hydrogeol J 14:926–941. https://doi.org/10.1007/s10040-005-0009-9
Goudjal Y, Zamoum M, Meklat A, Sabaou N, Mathieu F, Zitouni A (2015) Plant-growth-promoting potential of endosymbiotic actinobacteria isolated from sand truffles (Terfezia leonisTul.) of the algerian sahara. Ann Microbiol 66:91–100. https://doi.org/10.1007/s13213-015-1085-2
Green SA, Blough NV (1994) Optical absorption and fluorescence properties of chromophoric dissolved organic matter in natural waters. Limnol Oceanogr 39:1903–1916. https://doi.org/10.2307/2838396
Hallbourg RR, Delfino JJ, Miller WL (1992) Organic priority pollutants in groundwater and surface water at three landfills in north central Florida. Water Air Soil Pollut 65:307–322. https://doi.org/10.1007/BF00479894
He Y, Men B, Yang XF, Li YX, Xu H, Wang DS (2019) Relationship between heavy metals and dissolved organic matter released from sediment by bioturbation/bioirrigation. J Environ Sci 75:216–223. https://doi.org/10.1016/j.jes.2018.03.031
He XS, Zhang YL, Liu ZH, Wei D, Liang G, Liu HT, Xi BD, Huang ZB, Ma Y, Xing BS (2020) Interaction and coexistence characteristics of dissolved organic matter with toxic metals and pesticides in shallow groundwater. Environ Pollut 258:113736. https://doi.org/10.1016/j.envpol.2019.113736
Helms JR, Stubbins A, Ritchie JD, Minor E (2008) Absorption spectral slopes and slope ratios as indicators of molecular weight, source, and photobleaching of chromophoric dissolved organic matter. Limnol Oceanogr 53:955–969. https://doi.org/10.4319/lo.2008.53.3.0955
Hoehn E, Scholtis A (2011) Exchange between a river and groundwater, assessed with hydrochemical data. Hydrol Earth Syst Sci 7:983–988. https://doi.org/10.5194/hess-15-983-2011
Hofmann R, Griebler C (2018) DOM and bacterial growth efficiency in oligotrophic groundwater: absence of priming and co-limitation by organic carbon and phosphorus. Aquat Microb Ecol 81:55–71. https://doi.org/10.3354/ame01862
Hong HS, Yang LY, Guo WD, Wang FL, Yu XX (2012) Characterization of dissolved organic matter under contrasting hydrologic regimes in a subtropical watershed using PARAFAC model. Biogeochemistry 109:163–174. https://doi.org/10.2307/41490551
Huang SB, Wang YX, Ma T, Tong L, Wang YY, Liu CR, Zhao L (2015) Linking groundwater dissolved organic matter to sedimentary organic matter from a fluvio-lacustrine aquifer at Jianghan Plain, China by EEM-PARAFAC and hydrochemical analyses. Sci Total Environ 529:131–139. https://doi.org/10.1016/j.scitotenv.2015.05.051
Hug LA, Thomas BC, Brown CT, Frischkorn KR, Williams KH, Tringe SG, Banfield JF (2015) Aquifer environment selects for microbial species cohorts in sediment and groundwater. ISME J 9:1846–1856. https://doi.org/10.1038/ismej.2015.2
Inamdar S, Finger N, Singh S, Mitchell M, Levia D, Bais H, Scott D, McHale P (2012) Dissolved organic matter (DOM) concentration and quality in a forested mid-Atlantic watershed, USA. Biogeochemistry 108:55–76. https://doi.org/10.1007/s10533-011-9572-4
Jansson M, Persson L, AndréMDR JR, Tranvik LJ (2007) Terrestrial carbon and intraspecific size-variation shape lake ecosystems. Trends Ecol Evol 22:316–322. https://doi.org/10.1016/j.tree.2007.02.015
Ji B, Qin H, Guo SD, Chen W, Zhang XC, Liang JC (2018) Bacterial communities of four adjacent fresh lakes at different trophic status. Ecotox Environ Safe 157:388–394. https://doi.org/10.1016/j.ecoenv.2018.03.086
Konikow LF, Kendy E (2005) Groundwater depletion: a global problem. Hydrogeol J 13:317–320. https://doi.org/10.1007/s10040-004-0411-8
Langille MGI, Zaneveld J, Caporaso JG, McDonald D, Knights D, Reyes JA, Clemente JC, Burkepile DE, Vega Thurber RL, Knight R, Beiko RG, Huttenhower C (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
Lapworth DJ, Gooddy DC, Butcher AS, Morns BL (2008) Tracing groundwater flow and sources of organic carbon in sandstone aquifers using fluorescence properties of dissolved organic matter (DOM). Appl Geochem 23:3384–3390. https://doi.org/10.1016/j.apgeochem.2008.07.011
Li JX, Wang YX, Guo W, Xie XJ, Zhang LP, Liu YQ, Kong SQ (2014) Iodine mobilization in groundwater system at Datong basin, China: evidence from hydrochemistry and fluorescence characteristics. Sci Total Environ 468–469:738–745. https://doi.org/10.1016/j.scitotenv.2013.08.092
Li L, Wang M, Xing HX, Ge WY, Li LE, Yu C, Jia JY (2020) Analysis on groundwater environmental isotopic composition and evolution in northern Taihu Lake. Yangtze River 51:41–46. https://doi.org/10.16232/j.cnki.1001-4179.2020.05.007
Mallén G, Maloszewski P, Flynn R, Rossi P, Engel M, Seiler KP (2004) Determination of bacterial and viral transport parameters in a gravel aquifer assuming linear kinetic sorption and desorption. J Hydrol 306:21–36. https://doi.org/10.1016/j.jhydrol.2004.08.033
Mcknight DM, Boyer EW, Westerhoff PK, Doran PT, Kulbe T, Andersen DT (2001) Spectrofluorometric characterization of dissolved organic matter for indication of precursor organic material and aromaticity. Limnol Oceanogr 46:38–48. https://doi.org/10.4319/lo.2001.46.1.0038
McMahon KD, Read EK (2013) Microbial contributions to phosphorus cycling in eutrophic lakes and wastewater. Annu Rev Microbiol 67:199–219. https://doi.org/10.1146/annurev-micro-092412-155713
Murphy KR, Ruiz GM, Dunsmuir WTM, Waite TD (2006) Optimized parameters for fluorescence-based verification of ballast water exchange by ships. Environ Sci Technol 40:2357–2362. https://doi.org/10.1021/es0519381
Murphy KR, Stedmon CA, Waite TD, Ruiz GM (2008) Distinguishing between terrestrial and autochthonous organic matter sources in marine environments using fluorescence spectroscopy. Mar Chem 108:40–58. https://doi.org/10.1016/j.marchem.2007.10.003
Ogata H, Goto S, Sato K, Fujibuchi W, Bono H, Kanehisa M (1999) KEGG: kyoto encyclopedia of genes and genomes. Nucleic Acids Res 27:29–34. https://doi.org/10.1093/nar/27.1.29
Ohno T, Bro R (2006) Dissolved organic matter characterization using multiway spectral decomposition of fluorescence landscapes. Soil Sci Soc Am J 70:2028–2037. https://doi.org/10.2136/sssaj2006.0005
Ohno T, Chorover J, Omoike A, Hunt J (2007) Molecular weight and humification index as predictors of adsorption for plant- and manure-derived dissolved organic matter to goethite. Eur J Soil Sci 58:125–132. https://doi.org/10.1111/j.1365-2389.2006.00817.x
Papirio S, Zou G, Ylinen A, DiCapua F, Pirozzi F, Puhakka JA (2014) Effect of arsenic on nitrification of simulated mining water. Bioresour Technol 164:149–154. https://doi.org/10.1016/j.biortech.2014.04.072
Peng YK, Yue DM, Xiao L, Qian B (2017) Temporal variation and co-occurrence patterns of bacterial communities in eutrophic lake Taihu, China. Geomicrobiol J (2018) https://doi.org/10.1029/2012JG002072, 2012.
Peter S, Shen Y, Kaiser K, Benner R, Durisch-Kaiser E (2012) Bioavailability and diagenetic state of dissolved organic matter in riparian groundwater. J Geophys Res-Atmos 117:G04006. https://doi.org/10.1029/2012JG002072
Pifer AD, Fairey JL (2012) Improving on SUVA 254 using fluorescence-PARAFAC analysis and asymmetric flow-field flow fractionation for assessing disinfection byproduct formation and control. Water Res 46:2927–2936. https://doi.org/10.1016/j.watres.2012.03.002
Pizzeghello D, Zanella A, Carletti P, Nardi S (2006) Chemical and biological characterization of dissolved organic matter from silver fir and beech forest soils. Chemosphere 65:190–200. https://doi.org/10.1016/j.chemosphere.2006.03.001
Qin BQ, Xu PZ, Wu Q, Luo LC, Zhang YL (2007) Environmental issues of Lake Taihu, China. Hydrobiologia 581:3–14. https://doi.org/10.1007/s10750-006-0521-5
Ren XY, Zeng GM, Tang L, Wang JJ, Wan J, Liu YN, Yu JF, Yi H, Ye SJ, Deng R (2018) Sorption, transport and biodegradation–an insight into bioavailability of persistent organic pollutants in soil. Sci Total Environ 610–611:1154–1163. https://doi.org/10.1016/j.scitotenv.2017.08.089
Servin JA, Herbold CW, Skophammer RG, Lake JA (2008) Evidence excluding the root of the tree of life from the actinobacteria. Mol Biol Evol 25:1–4. https://doi.org/10.1093/molbev/msm249
Shen Y, Chapelle FH, Strom EW, Benner R (2015) Origins and bioavailability of dissolved organic matter in groundwater. Biogeochemistry 122:61–78. https://doi.org/10.1007/s10533-014-0029-4
Simek K, Kasalicky V, Zapomelova E, Hornak K (2011) Alga-derived substrates select for distinct Betaproteobacterial lineages and contribute to niche separation in Limnohabitans strains. Appl Environ Microbiol 77:7307–7315. https://doi.org/10.1128/AEM.05107-11
Sinton LW, Finlay RK, Pang L, Scott DM (1997) Transport of bacteria and bacteriophages in irrigated effluent into and through an alluvial gravel aquifer. Water Air Soil Pollut 98:17–42. https://doi.org/10.1007/BF02128648
Sinton LW, Mackenzie ML, Karki N, Dann RL, Pang LP, Close ME (2012) Transport of Escherichia coli and F-RNA bacteriophages in a 5-M column of saturated, heterogeneous gravel. Water Air Soil Pollut 223:2347–2360. https://doi.org/10.1016/j.jconhyd.2010.06.007
Stedmon CA, Markager S, Bro R (2003) Tracing dissolved organic matter in aquatic environments using a new approach to fluorescence spectroscopy. Mar Chem 82:239–254. https://doi.org/10.1016/S0304-4203(03)00072-0
Su XM, Steinman AD, Tang XM, Xue QG, Zhao YY, Xie LQ (2017) Response of bacterial communities to cyanobacterial harmful algal blooms in Lake Taihu, China. Harmful Algae 68:168–177. https://doi.org/10.1016/j.hal.2017.08.007
Taylor LH, Latham SM, Woolhouse MEJ (2001) Risk factors for human disease emergence. Philos Trans R Soc B-Biol Sci 356:983–989. https://doi.org/10.1098/rstb.2001.0888
Vázquez-Suné E, Sánchez-Vila X, Carrera J (2005) Introductory review of specific factors influencing urban groundwater, an emerging branch of hydrogeology, with reference to Barcelona, Spain. Hydrogeol J 13:522–533. https://doi.org/10.1007/s10040-004-0360-2
Wang SH, Wang WW, Chen JY, Zhang B, Zhao L, Jiang X (2020) Characteristics of dissolved organic matter and its role in lake eutrophication at the early stage of algal blooms–a case study of lake Taihu. China Water 12:2278. https://doi.org/10.3390/w12082278
Wang C, Guo WD, Guo ZR, Wei J, Zhang B, Ma ZR (2013) Characterization of dissolved organic matter in groundwater from the coastal Dagu river watershed, China using fluorescence excitation-emission matrix spectroscopy. Spectrosc Spectr Anal 33:2460–2465. https://doi.org/10.3964/j.issn.1000-0593(2013)09-2460-06
Waterbury JB, Watson SW, Guillard R, Brand LE (1979) Widespread occurrence of a unicellular, marine, planktonic, cyanobacterium. Nature 277:293–294. https://doi.org/10.1038/277293a0
Wei MJ, Gao C, Zhou YJ, Duan PF, Li M (2019) Variation in spectral characteristics of dissolved organic matter in inland rivers in various trophic states, and their relationship with phytoplankton. Ecol Indic 104:321–332. https://doi.org/10.1016/j.ecolind.2019.05.020
Xu Y, Xu YP, Wu L, Wang Q, Gao B, Zhou Y (2018) Characteristics of shallow groundwater and its influences in plain river network region of Taihu Basin. J Lake Sci 30:464–471. https://doi.org/10.18307/2018.0218
Yao B, Hu CM, Liu QQ (2016) Fluorescent components and spatial patterns of chromophoric dissolved organic matters in Lake Taihu, a large shallow eutrophic lake in China. Environ Sci Pollut Res 23:23057–23070. https://doi.org/10.1007/s11356-016-7510-7
Zhang W, Zhou YQ, Jeppesen E, Wang LQ, Tan HX, Zhang JY (2019) Linking heterotrophic bacterioplankton community composition to the optical dynamics of dissolved organic matter in a large eutrophic Chinese lake. Sci Total Environ 679:136–147. https://doi.org/10.1016/j.scitotenv.2019.05.055
Zhang L, Fang WK, Li XC, Gao G, Jiang JH (2020a) Linking bacterial community shifts with changes in the dissolved organic matter pool in a eutrophic lake. Sci Total Environ 719:137387–137399. https://doi.org/10.1016/j.scitotenv.2020.137387
Zhang L, Fang WK, Li XC, Lu WX, Li J (2020b) Strong linkages between dissolved organic matter and the aquatic bacterial community in an urban river. Water Res 184:116089–117000. https://doi.org/10.1016/j.watres.2020.116089
Zhao DY, Xu HM, Zeng J, Cao XY, Huang R, Shen F, Yu ZB (2017) Community composition and assembly processes of the free-living and particle-attached bacteria in Taihu Lake. FEMS Microbiol Ecol 93:fix06. https://doi.org/10.1093/femsec/fix062.
Zhou L, Zhou YQ, Tang XM, Zhang YL, Jang K, Székely AJ, Jeppesen E (2021) Resource aromaticity affects bacterial community successions in response to different sources of dissolved organic matter. Water Res 190:116776–116788. https://doi.org/10.1016/j.watres.2020.116776
Acknowledgements
This work was supported by the National Natural Science Foundation of China (51979236 and 41771308) and the Open Fund of State Key Laboratory of Eco-hydraulics in Northwest Arid Region (2019KFKT-1). ML was also funded as Tang Scholar by Cyrus Tang Foundation and Northwest A&F University. The data that support the findings of this study are available from the corresponding author upon request.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Additional information
Handling Editor: Télesphore Sime-Ngando.
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.
Rights and permissions
About this article
Cite this article
Ma, N., Gao, L., Zhang, Y. et al. Spatial variation in bacterial community and dissolved organic matter composition in groundwater near a eutrophic lake. Aquat Ecol 56, 555–571 (2022). https://doi.org/10.1007/s10452-021-09926-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10452-021-09926-6