{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,16]],"date-time":"2026-09-16T06:05:03Z","timestamp":1789538703052,"version":"build-2803163510"},"reference-count":42,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2026,9,16]],"date-time":"2026-09-16T00:00:00Z","timestamp":1789516800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Microbiol."],"abstract":"<jats:sec>\n                    <jats:title>Objective<\/jats:title>\n                    <jats:p>Petroleum-hydrocarbon plumes in groundwater are shaped by hydrological transport, redox conditions, and indigenous microbial activity. However, it remains unclear whether spatial differences among groundwater microbiomes primarily reflect physical separation among wells or ecological reorganization associated with distinct attenuation states within a plume.<\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Methods<\/jats:title>\n                    <jats:p>We integrated hydrogeological context, petroleum-hydrocarbon concentrations, hydrochemical variables, and shotgun-metagenomic profiles from 15 groundwater monitoring wells at a petroleum-hydrocarbon-impacted site. Community beta diversity, spatial and functional distance relationships, permutation-based group tests, and exploratory composite indices of natural attenuation potential and taxonomic-functional diversity were evaluated.<\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Results<\/jats:title>\n                    <jats:p>\n                      Genus-level community dissimilarity increased with estimated spatial distance (Mantel r\u202f=\u202f0.240,\n                      <jats:italic>p<\/jats:italic>\n                      \u202f=\u202f0.034), but was more strongly associated with functional-module dissimilarity (r\u202f=\u202f0.670,\n                      <jats:italic>p<\/jats:italic>\n                      \u202f=\u202f0.001). Biodegradation potential remained associated with community dissimilarity after controlling for spatial distance (partial Mantel\n                      <jats:italic>r<\/jats:italic>\n                      \u202f=\u202f0.428,\n                      <jats:italic>p<\/jats:italic>\n                      \u202f=\u202f0.001). Operational attenuation states explained 35.4% of genus-level compositional variation (PERMANOVA\n                      <jats:italic>p<\/jats:italic>\n                      \u202f=\u202f0.008). High natural attenuation potential and high taxonomic-functional diversity occurred in partly distinct wells.\n                    <\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Conclusion<\/jats:title>\n                    <jats:p>The results indicate that groundwater microbiome turnover within the plume is spatially structured but is more closely coupled to functional reorganization than to distance alone. Joint consideration of hydrological setting, microbial degradation potential, and functional diversity may improve groundwater natural-attenuation assessment.<\/jats:p>\n                  <\/jats:sec>","DOI":"10.3389\/fmicb.2026.1938677","type":"journal-article","created":{"date-parts":[[2026,9,16]],"date-time":"2026-09-16T05:33:07Z","timestamp":1789536787000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":0,"title":["Functional organization outweighs spatial separation in structuring microbial communities across a petroleum-hydrocarbon groundwater plume"],"prefix":"10.3389","volume":"17","author":[{"given":"Ruihuan","family":"Zhang","sequence":"first","affiliation":[{"name":"School of Environment, Tsinghua University","place":["Beijing, China"]},{"name":"State Key Laboratory of Regional Environment and Sustainability, Tsinghua University","place":["Beijing, China"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yu","family":"Chen","sequence":"additional","affiliation":[{"name":"School of Environment, Tsinghua University","place":["Beijing, China"]},{"name":"State Key Laboratory of Regional Environment and Sustainability, Tsinghua University","place":["Beijing, China"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Deyi","family":"Hou","sequence":"additional","affiliation":[{"name":"School of Environment, Tsinghua University","place":["Beijing, China"]},{"name":"State Key Laboratory of Regional Environment and Sustainability, Tsinghua University","place":["Beijing, China"]}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1965","published-online":{"date-parts":[[2026,9,16]]},"reference":[{"key":"ref1","doi-asserted-by":"publisher","first-page":"1522714","DOI":"10.3389\/fmicb.2025.1522714","article-title":"Spatial and temporal groundwater biogeochemical variability help inform subsurface connectivity within a high-altitude alpine catchment (Riale di Ronco, Switzerland)","volume":"16","author":"Acciardo","year":"2025","journal-title":"Front. Microbiol."},{"key":"ref2","doi-asserted-by":"publisher","first-page":"2860","DOI":"10.1128\/AEM.01752-06","article-title":"The microbial community structure in petroleum-contaminated sediments corresponds to geophysical signatures","volume":"73","author":"Allen","year":"2007","journal-title":"Appl. Environ. Microbiol."},{"key":"ref3","doi-asserted-by":"publisher","first-page":"2251","DOI":"10.1093\/bioinformatics\/btz859","article-title":"KofamKOALA: KEGG Ortholog assignment based on profile HMM and adaptive score threshold","volume":"36","author":"Aramaki","year":"2020","journal-title":"Bioinformatics"},{"key":"ref4","doi-asserted-by":"publisher","first-page":"1593892","DOI":"10.3389\/fmicb.2025.1593892","article-title":"Examination of coal combustion management sites for microbiological and chemical signatures of groundwater impacts","volume":"16","author":"Bagwell","year":"2025","journal-title":"Front. Microbiol."},{"key":"ref5","doi-asserted-by":"publisher","first-page":"387","DOI":"10.1016\/S0169-7722(01)00175-9","article-title":"Progression of natural attenuation processes at a crude oil spill site: II. Controls on spatial distribution of microbial populations","volume":"53","author":"Bekins","year":"2001","journal-title":"J. Contam. Hydrol."},{"key":"ref6","doi-asserted-by":"publisher","first-page":"2114","DOI":"10.1093\/bioinformatics\/btu170","article-title":"Trimmomatic: a flexible trimmer for Illumina sequence data","volume":"30","author":"Bolger","year":"2014","journal-title":"Bioinformatics"},{"key":"ref7","doi-asserted-by":"publisher","first-page":"115314","DOI":"10.1016\/j.watres.2019.115314","article-title":"Investigation into the microbial communities and associated crude oil-contamination along a gulf war impacted groundwater system in Kuwait","volume":"170","author":"Bruckberger","year":"2020","journal-title":"Water Res."},{"key":"ref8","doi-asserted-by":"publisher","first-page":"41","DOI":"10.1007\/PL00010973","article-title":"The significance of microbial processes in hydrogeology and geochemistry","volume":"8","author":"Chapelle","year":"2000","journal-title":"Hydrogeol. J."},{"key":"ref9","doi-asserted-by":"publisher","first-page":"126","DOI":"10.1016\/j.jhydrol.2013.09.027","article-title":"Application of natural attenuation for the control of petroleum hydrocarbon plume: mechanisms and effectiveness evaluation","volume":"505","author":"Chiu","year":"2013","journal-title":"J. Hydrol."},{"key":"ref10","doi-asserted-by":"publisher","first-page":"30","DOI":"10.1111\/gwmr.12536","article-title":"Understanding the evolution of groundwater-contaminant plume chemistry emanating from legacy contaminant sources: an example from a long-term crude oil spill","volume":"42","author":"Cozzarelli","year":"2022","journal-title":"Ground Water Monit. Remediat."},{"key":"ref11","doi-asserted-by":"publisher","first-page":"2601","DOI":"10.1021\/es051748q","article-title":"Phylogenetic and functional biomarkers as indicators of bacterial community responses to mixed-waste contamination","volume":"40","author":"Fields","year":"2006","journal-title":"Environ. Sci. Technol."},{"key":"ref12","doi-asserted-by":"publisher","first-page":"669","DOI":"10.1099\/ijs.0.02298-0","article-title":"Rhodoferax ferrireducens sp. nov., a psychrotolerant, facultatively anaerobic bacterium that oxidizes acetate with the reduction of Fe(III)","volume":"53","author":"Finneran","year":"2003","journal-title":"Int. J. Syst. Evol. Microbiol."},{"key":"ref13","doi-asserted-by":"publisher","first-page":"1957","DOI":"10.1098\/rstb.2003.1380","article-title":"Groundwater: the processes and global significance of aquifer degradation","volume":"358","author":"Foster","year":"2003","journal-title":"Philos. Trans. R. Soc. Lond. Ser. B Biol. Sci."},{"key":"ref14","doi-asserted-by":"publisher","first-page":"649","DOI":"10.1111\/j.1365-2427.2008.02013.x","article-title":"Microbial biodiversity in groundwater ecosystems","volume":"54","author":"Griebler","year":"2009","journal-title":"Freshw. Biol."},{"key":"ref15","doi-asserted-by":"publisher","first-page":"5898","DOI":"10.1111\/1462-2920.16219","article-title":"Ecological processes differ in community assembly of Archaea, Bacteria and eukaryotes in a biogeographical survey of groundwater habitats in the Quebec region (Canada)","volume":"24","author":"Groult","year":"2022","journal-title":"Environ. Microbiol."},{"key":"ref16","doi-asserted-by":"publisher","first-page":"118767","DOI":"10.1016\/j.watres.2022.118767","article-title":"A metagenomic portrait of the microbial community responsible for two decades of bioremediation of poly-contaminated groundwater","volume":"221","author":"Hauptfeld","year":"2022","journal-title":"Water Res."},{"key":"ref17","doi-asserted-by":"publisher","first-page":"660","DOI":"10.1038\/ismej.2009.154","article-title":"Metagenomic insights into evolution of a heavy metal-contaminated groundwater microbial community","volume":"4","author":"Hemme","year":"2010","journal-title":"ISME J."},{"key":"ref18","doi-asserted-by":"publisher","first-page":"1205","DOI":"10.3389\/fmicb.2015.01205","article-title":"Comparative metagenomics reveals impact of contaminants on groundwater microbiomes","volume":"6","author":"Hemme","year":"2015","journal-title":"Front. Microbiol."},{"key":"ref19","doi-asserted-by":"publisher","first-page":"3815","DOI":"10.1128\/AEM.71.7.3815-3825.2005","article-title":"Dynamics of an oligotrophic bacterial aquifer community during contact with a groundwater plume contaminated with benzene, toluene, ethylbenzene, and xylenes: an in situ mesocosm study","volume":"71","author":"Hendrickx","year":"2005","journal-title":"Appl. Environ. Microbiol."},{"key":"ref20","doi-asserted-by":"publisher","first-page":"2644","DOI":"10.1128\/AEM.02332-06","article-title":"Oil field souring control by nitrate-reducing Sulfurospirillum spp. that outcompete sulfate-reducing bacteria for organic electron donors","volume":"73","author":"Hubert","year":"2007","journal-title":"Appl. Environ. Microbiol."},{"key":"ref21","doi-asserted-by":"publisher","first-page":"7564","DOI":"10.1038\/s41598-018-25961-0","article-title":"Metagenomic profiling for assessing microbial diversity and microbial adaptation to degradation of hydrocarbons in two south African petroleum-contaminated water aquifers","volume":"8","author":"Kachienga","year":"2018","journal-title":"Sci. Rep."},{"key":"ref22","doi-asserted-by":"publisher","first-page":"27","DOI":"10.1093\/nar\/28.1.27","article-title":"KEGG: Kyoto encyclopedia of genes and genomes","volume":"28","author":"Kanehisa","year":"2000","journal-title":"Nucleic Acids Res."},{"key":"ref23","doi-asserted-by":"publisher","first-page":"2799","DOI":"10.1128\/AEM.67.6.2799-2809.2001","article-title":"Attached and unattached microbial communities in a simulated basalt aquifer under fracture- and porous-flow conditions","volume":"67","author":"Lehman","year":"2001","journal-title":"Appl. Environ. Microbiol."},{"key":"ref24","doi-asserted-by":"publisher","first-page":"1674","DOI":"10.1093\/bioinformatics\/btv033","article-title":"MEGAHIT: an ultra-fast single-node solution for large and complex metagenomics assembly via succinct de Bruijn graph","volume":"31","author":"Li","year":"2015","journal-title":"Bioinformatics"},{"key":"ref25","doi-asserted-by":"publisher","first-page":"936","DOI":"10.1038\/s41559-018-0519-1","article-title":"Function and functional redundancy in microbial systems","volume":"2","author":"Louca","year":"2018","journal-title":"Nat. Ecol. Evol."},{"key":"ref26","doi-asserted-by":"publisher","first-page":"e104","DOI":"10.7717\/peerj-cs.104","article-title":"Bracken: estimating species abundance in metagenomics data","volume":"3","author":"Lu","year":"2017","journal-title":"PeerJ Comput. Sci."},{"key":"ref27","doi-asserted-by":"publisher","first-page":"156768","DOI":"10.1016\/j.scitotenv.2022.156768","article-title":"Subsurface microbial communities as a tool for characterizing regional-scale groundwater flow","volume":"842","author":"Merino","year":"2022","journal-title":"Sci. Total Environ."},{"key":"ref28","volume-title":"Water Quality - Determination of Total Organic carbon - Combustion Oxidation non-dispersive Infrared Absorption Method (HJ 501\u20132009)","year":"2009"},{"key":"ref29","volume-title":"Water Quality - Determination of Volatile Organic Compounds - Purge and trap\/gas Chromatography-mass Spectrometry (HJ 639\u20132012)","year":"2012"},{"key":"ref30","volume-title":"Water Quality - Determination of Inorganic Anions - Ion Chromatography (HJ 84\u20132016)","year":"2016"},{"key":"ref31","volume-title":"Water Quality - Determination of Extractable petroleum Hydrocarbons (C10-C40) - Gas Chromatography (HJ 894\u20132017)","year":"2017"},{"key":"ref32","volume-title":"Water Quality - Determination of pH Value - Electrode Method (HJ 1147\u20132020)","year":""},{"key":"ref33","volume-title":"Technical Specifications for Environmental Monitoring of groundwater (HJ 164\u20132020)","year":""},{"key":"ref34","doi-asserted-by":"publisher","first-page":"490","DOI":"10.1038\/s41564-023-01573-x","article-title":"Environmental stress mediates groundwater microbial community assembly","volume":"9","author":"Ning","year":"2024","journal-title":"Nat. Microbiol."},{"key":"ref35","doi-asserted-by":"publisher","first-page":"2068","DOI":"10.1093\/bioinformatics\/btu153","article-title":"Prokka: rapid prokaryotic genome annotation","volume":"30","author":"Seemann","year":"2014","journal-title":"Bioinformatics"},{"key":"ref36","doi-asserted-by":"publisher","first-page":"2613","DOI":"10.1128\/AEM.01955-08","article-title":"Characterization of a polycyclic aromatic hydrocarbon degradation gene cluster in a phenanthrene-degrading Acidovorax strain","volume":"75","author":"Singleton","year":"2009","journal-title":"Appl. Environ. Microbiol."},{"key":"ref37","doi-asserted-by":"publisher","first-page":"114816","DOI":"10.1016\/j.envres.2022.114816","article-title":"The collaborative monitored natural attenuation (CMNA) of soil and groundwater pollution in large petrochemical enterprises: a case study","volume":"216","author":"Song","year":"2023","journal-title":"Environ. Res."},{"key":"ref38","doi-asserted-by":"publisher","first-page":"1026","DOI":"10.1038\/nbt.3988","article-title":"MMseqs2 enables sensitive protein sequence searching for the analysis of massive data sets","volume":"35","author":"Steinegger","year":"2017","journal-title":"Nat. Biotechnol."},{"key":"ref39","doi-asserted-by":"publisher","first-page":"116","DOI":"10.1144\/qjegh2023-116","article-title":"Natural attenuation of dissolved petroleum fuel constituents in a fractured chalk aquifer: contaminant mass balance with probabilistic analysis","volume":"57","author":"Thornton","year":"2024","journal-title":"Q. J. Eng. Geol. Hydrogeol."},{"key":"ref40","doi-asserted-by":"publisher","first-page":"792","DOI":"10.1128\/AEM.01951-07","article-title":"Depth-resolved quantification of anaerobic toluene degraders and aquifer microbial community patterns in distinct redox zones of a tar oil contaminant plume","volume":"74","author":"Winderl","year":"2008","journal-title":"Appl. Environ. Microbiol."},{"key":"ref41","doi-asserted-by":"publisher","first-page":"257","DOI":"10.1186\/s13059-019-1891-0","article-title":"Improved metagenomic analysis with kraken 2","volume":"20","author":"Wood","year":"2019","journal-title":"Genome Biol."},{"key":"ref42","doi-asserted-by":"publisher","first-page":"115341","DOI":"10.1016\/j.watres.2019.115341","article-title":"Environmental selection shapes the formation of near-surface groundwater microbiomes","volume":"170","author":"Yan","year":"2020","journal-title":"Water Res."}],"container-title":["Frontiers in Microbiology"],"original-title":[],"link":[{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fmicb.2026.1938677\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,9,16]],"date-time":"2026-09-16T05:33:09Z","timestamp":1789536789000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fmicb.2026.1938677\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2026,9,16]]},"references-count":42,"alternative-id":["10.3389\/fmicb.2026.1938677"],"URL":"https:\/\/doi.org\/10.3389\/fmicb.2026.1938677","relation":{},"ISSN":["1664-302X"],"issn-type":[{"value":"1664-302X","type":"electronic"}],"subject":[],"published":{"date-parts":[[2026,9,16]]},"article-number":"1938677"}}