Abstract
The 2010 Deepwater Horizon disaster remains one of the largest oil spills in history. This event caused significant damage to coastal ecosystems, the full extent of which has yet to be fully determined. Crude oil contains toxic heavy metals and substances such as polycyclic aromatic hydrocarbons that are detrimental to some microbial species and may be used as food and energy resources by others. As a result, oil spills have the potential to cause significant shifts in microbial communities. This study assessed the impact of oil contamination on the function of endophytic microbial communities associated with saltmarsh cordgrass (Spartina alterniflora). Soil samples were collected from two locations in coastal Louisiana, USA: one severely affected by the Deepwater Horizon oil spill and one relatively unaffected location. Spartina alterniflora seedlings were grown in both soil samples in greenhouses, and GeoChip 5.0 was used to evaluate the endophytic microbial metatranscriptome shifts in response to host plant oil exposure. Oil exposure was associated with significant shifts in microbial gene expression in functional categories related to carbon cycling, virulence, metal homeostasis, organic remediation, and phosphorus utilization. Notably, significant increases in expression were observed in genes related to metal detoxification with the exception of chromium, and both significant increases and decreases in expression were observed in functional gene subcategories related to hydrocarbon metabolism. These findings show that host oil exposure elicits multiple changes in gene expression from their endophytic microbial communities, producing effects that may potentially impact host plant fitness.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
Data are publicly available through the Gulf of Mexico Research Initiative Information & Data Cooperative (GRIIDC) at https://data.gulfresearchinitiative.org (https://doi.org/10.7266/n7-rzxc-4x96). All raw data are publicly available on the NCBI SRA database (Accession Number: GSE148431) and upon request.
Code availability
Not applicable.
References
Alvarez M, Ferreira de Carvalho J, Salmon A, Ainouche ML, Cavé-Radet A, El Amrani A, Foster TE, Moyer S, Richards CL (2018) Transcriptome response of the foundation plant Spartina alterniflora to the Deepwater Horizon oil spill. Mol Ecol 27(14):2986–3000. https://doi.org/10.1111/mec.14736
Bååth E (1989) Effects of heavy metals in soil on microbial processes and populations (a review). Water Air Soil Pollut 47:335–379. https://doi.org/10.1007/BF00279331
Brundrett M (2004) Diversity and classification of mycorrhizal associations. Biol Rev 79:473–495. https://doi.org/10.1017/S1464793103006316
Cong J, Liu X, Lu H, Xu H, Li Y, Deng Y, Li D, Zhang Y (2015) Analyses of the influencing factors of soil microbial functional gene diversity in tropical rainforest based on GeoChip 5.0. Genom Data 5:397–398. https://doi.org/10.1016/j.gdata.2015.07.010
Cunliffe M, Kertesz MA (2006) Effect of Sphingobium yanoikuyae B1 inoculation on bacterial community dynamics and polycyclic aromatic hydrocarbon degradation in aged and freshly PAH-contaminated soils. Environ Pollution 144(1):228–237. https://doi.org/10.1016/j.envpol.2005.12.026
Deepwater Horizon Natural Resource Damage Assessment Trustees (2016). Deepwater horizon oil spill: final programmatic damage assessment and restoration plan and final programmatic environmental impact statement. http://www.gulfspillrestoration.noaa.gov/restoration-planning/gulf-plan
Doyle SM, Whitaker EA, De Pascuale V, Wade TL, Knap AH, Santschi PH, Quigg A, and Sylvan JB (2018) Rapid formation of microbe-oil aggregates and changes in community composition in coastal surface water following exposure to oil and the dispersant corexit. Front Microbio 9:689. https://doi.org/10.3389/fmicb.2018.00689
Edwards KR, Mills KP (2005) Aboveground and belowground productivity of Spartina alterniflora (smooth cordgrass) in natural and created Louisiana salt marshes. Estuaries 28(2):252–265. https://doi.org/10.1007/BF02732859
Ghosal D, Ghosh S, Dutta T, Ahn Y (2016) Current state of knowledge in microbial degradation of polycyclic aromatic hydrocarbons (PAHS): a review. Front Microbiol 7:1369. https://doi.org/10.3389/fmicb.2016.01369
Giller KE, Witter E, Mcgrath SP (1998) Toxicity of heavy metals to microorganisms and microbial processes in agricultural soils: a review. Soil Biol Biochem 30(10-11):1389-1414.https://doi.org/10.1016/S0038-0717(97)00270-8
Groudeva VI, Groudev SN, Doycheva AS (2001) Bioremediation of waters contaminated with crude oil and toxic heavy metals. Int J Miner Process 62:293–299. https://doi.org/10.1016/S0301-7516(00)00060-0
Kandalepas D, Blum MJ, Van Bael SA (2015) Shifts in symbiotic endophyte communities of a foundational salt marsh grass following oil exposure from the Deepwater Horizon oil spill. PLoS ONE. https://doi.org/10.1371/journal.pone.0122378
Khare E, Mishra J, Arora NK (2018) Multifaceted interactions between endophytes and plant: developments and prospects. Front Microbiol. https://doi.org/10.3389/fmicb.2018.02732
Krauss KW, Chambers JL, Allen JA (1998) Salinity effects and differential germination of several half-sib families of bald cypress from different seed sources. New For 15:53–68. https://doi.org/10.1023/A:1006572609171
Leitenmaier B, Küpper H (2013) Compartmentation and complexation of metals in hyperaccumulator plants. Front Plant Sci. https://doi.org/10.3389/fpls.2013.00374
Lin H, Tao S, Zuo Q, Coveney RM (2007) Uptake of polycyclic aromatic hydrocarbons by maize plants. Environ Pollut 148(2):614–619. https://doi.org/10.1016/j.envpol.2006.11.026
Liu Z, Liu J, Zhu Q, Wu W (2012) The weathering of oil after the Deepwater Horizon oil spill: insights from the chemical composition of the oil from the sea surface, salt marshes and sediments. Environ Res Lett 7:035302. https://doi.org/10.1088/1748-9326/7/3/035302
Liu H, Carvalhais LC, Crawford M, Singh E, Dennis PG, Pieterse CMJ, Schenk PM (2017) Inner plant values: diversity, colonization and benefits from endophytic bacteria. Front Microbiol 8:2552. https://doi.org/10.3389/fmicb.2017.02552
Liu J, Zhang Z, Sheng Y, Gao Y, Zhao Z (2018) Phenanthrene-degrading bacteria on root surfaces: a natural defense that protects plants from phenanthrene contamination. Plant Soil 425:335–350. https://doi.org/10.1007/s11104-018-3575-z
Liu W, Zhang Y, Chen X, Maung-Douglass K, Strong DR, Pennings SC (2020) Contrasting plant adaptation strategies to latitude in the native and invasive range of Spartina alterniflora. New Phytol 226:623–634. https://doi.org/10.1111/nph.16371
Luo S, Wan Y, Xiao X, Guo H, Chen L, Xi Q, Zeng G, Liu C, Chen J (2011) Isolation and characterization of endophytic bacterium LRE07 from cadmium hyperaccumulator Solanum nigrum L. and its potential for remediation. Appl Microbiol Biotechnol 89:1637–1644. https://doi.org/10.1007/s00253-010-2927-2
Maliszewska-Kordybach B, Smreczak B (2000) Ecotoxicological activity of soils polluted with polycyclic aromatic hydrocarbons (PAHs): effect on plants. Environ Tech 21:1099–1110. https://doi.org/10.1080/09593330.2000.9618996
McNutt MK, Camilli R, Crone TJ, Guthrie GD, Hsieh PA, Ryerson TB, Savas O, Shaffer F (2011) Review of flow rate estimates of the Deepwater Horizon oil spill. Proc Natl Acad Sci USA 109:20260–20267. https://doi.org/10.1073/pnas.1112139108
Neff JM, Stout SA, Gunster DG (2005) Ecological risk assessment of polycyclic aromatic hydrocarbons in sediments: Identifying sources and ecological hazard. Integr Environ Assess Manag 1:22–33. https://doi.org/10.1897/IEAM_2004a-016.1
Odukoya J, Lambert R, Sakrabani R (2019) Understanding the impacts of crude oil and its induced abiotic stresses on agrifood production: a review. Horticulturae 5(2):47. https://doi.org/10.3390/horticulturae5020047
Oksanen J, Guillaume BF, Friendly M, Kindt R, Legendre P, McGlinn D, Minchin PR, O'Hara RB, Simpson GL, Solymos P, Stevens MHH, Szoecs E, and Wagner H (2019) vegan: community ecology package. R package version 2.5-6. https://CRAN.R-project.org/package=vegan
Osuji LC, Onojake CM (2004) Trace heavy metals associated with crude oil: a case study of Ebocha-8 oil-spill-polluted site in Niger delta, Nigeria. Chem Biodivers 1:1708–1715. https://doi.org/10.1002/cbdv.200490129
R Core Team (2020) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. https://www.R-project.org/
Reddy CM, Arey JS, Seewald JS, Sylva SP, Lemkau KL, Nelson RK, Carmichael CA, McIntyre CP, Fenwick J, Ventura GT, Van Mooy BA, Camilli R (2012) Composition and fate of gas and oil released to the water column during the Deepwater Horizon oil spill. Proc Natl Acad Sci USA 109(50):20229–20234. https://doi.org/10.1073/pnas.1101242108
Redfern LK, Gunsch CK (2016) Endophytic phytoaugmentation: treating wastewater and runoff through augmented phytoremediation. Ind Biotechnol 12(2):83–90. https://doi.org/10.1089/ind.2015.0016
Reinhold-Hurek B, Hurek T (2011) Living inside plants: bacterial endophytes. Curr Opin Plant Biol 14(4):435–443. https://doi.org/10.1016/j.pbi.2011.04.004
Rodrigue M, Elango V, Curtis D, Collins A, Pardue JH (2020) Biodegradation of MC252 polycyclic aromatic hydrocarbons and alkenes in two coastal wetlands. Mar Pollut Bull 157:111319. https://doi.org/10.1016/j.marpolbul.2020.111319
Seneviratne M, Rajakaruna N, Rizwan M, Madawala HMSP, Ok YS, Vithanage M (2017) Heavy metal-induced oxidative stress on seed germination and seedling development: a critical review. Environ Geochem Health 41(4):1813–1831. https://doi.org/10.1007/s10653-017-0005-8
Sethy SK, Ghosh S (2013) Effect of heavy metals on germination of seeds. J Nat Sci Biol Med 4(2):272–275. https://doi.org/10.4103/0976-9668.116964
Schroeder PJ, Jenkins DG (2018) How robust are popular beta diversity indices to sampling error? Ecosphere 9(2):e02100. https://doi.org/10.1002/ecs2.2100
Shi Z, Yin H, Van Nostrand JD, Voordeckers JW, Tu Q, Deng Y, Yuan M, Zhou A, Zhang P, Xiao N, Ning D, He Z, Wu L, Zhou J (2019) Functional gene array-based ultrasensitive and quantitative detection of microbial populations in complex communities. mSystems. https://doi.org/10.1128/mSystems.00296-19
Tidwell LG, Allan SE, O’Connell SG, Hobbie KA, Smith BW, Anderson KA (2016) PAH and OPAH flux during the deepwater horizon incident. Environ Sci Technol 50(14):7489–7497. https://doi.org/10.1021/acs.est.6b02784
U.S. Coast Guard (2011) B.P. Deepwater Horizon Oil Spill: Incident Specific Preparedness Review (ISPR), Final Report. Department of Homeland Security, Washington, DC
Udo EJ, Fayemi AAA (1975) The effect of oil pollution of soil on germination, growth and nutrient uptake of corn. J Environ Qual 4(4):537–540. https://doi.org/10.2134/jeq1975.00472425000400040023x
Ugarelli K, Laas P, Stingl U (2019) The microbial communities of leaves and roots associated with turtle grass (Thalassia testudinum) and manatee grass (Syringodium filliforme) are distinct from seawater and sediment communities, but are similar between species and sampling sites. Microorg 7(1):4. https://doi.org/10.3390/microorganisms7010004
Vyas TK, Dave BP (2010) Effect of addition of nitrogen, phosphorus, and potassium fertilizers on biodegradation of crude oil by marine bacteria. Indian J Mar Sci 39(10):143–150
Wallace J, Laforest-Lapointe I, Kembel S (2018) Variation in the leaf and root microbiome of sugar maple (Acer saccharum) at an elevational range limit. PeerJ 6:e5293. https://doi.org/10.7717/peerj.5293
Wei N, Ashman TL (2018) The effects of host species and sexual dimorphism differ among root, leaf and flower microbiomes of wild strawberries in situ. Sci Rep 8:5195. https://doi.org/10.1038/s41598-018-23518-9
Xia L, Geng Q, An S (2020) Rapid genetic divergence of an invasive species, Spartina alterniflora, in China. Front Genet 11:284. https://doi.org/10.3389/fgene.2020.00284
Zengel S, Bernik BM, Rutherford N, Nixon Z, Michel J (2015) Heavily oiled salt marsh following the Deepwater Horizon oil spill, ecological comparisons of shoreline cleanup treatments and recovery. PLoS ONE 10:e0132324. https://doi.org/10.1371/journal.pone.0132324
Funding
This research was made possible in part by a grant from The Gulf of Mexico Research Initiative, and in part by Duke’s Superfund Research Center, the National Institute for Environmental Health Sciences under the Grant NIEHS P42-ES010356, and the National Science Foundation’s Graduate Research Fellowship Program (Grant No. DGE-1644868).
Author information
Authors and Affiliations
Contributions
Study design, grant procurement, and project organization were managed by CKG, SAVB, and EL. Greenhouse maintenance and sample collection were performed by SKF and BMB. Samples were processed by YK and PV. Computational analyses were completed by SDA and DBR. Assembly and writing of manuscript were completed by SDA. Figures were constructed by SDA, SKF, and DBR. Manuscript was edited by DBR and CKG.
Corresponding author
Ethics declarations
Conflict of interest
Not applicable.
Additional information
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
Addis, S.D., Formel, S.K., Kim, Y.J. et al. Alterations of endophytic microbial community function in Spartina alterniflora as a result of crude oil exposure. Biodegradation 33, 87–98 (2022). https://doi.org/10.1007/s10532-021-09968-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10532-021-09968-5