Abstract
Purpose
The coastal environment is a fragile ecosystem exposed to anthropogenic pressures, including pollution. Microbial ecology studies have demonstrated the importance of microbial metabolism in marine sediments to maintain nutrient cycling; however, recalcitrant contaminants such as polycyclic aromatic hydrocarbons (PAHs) could affect these microbial communities. This study aimed to investigate the diversity of microbial communities on marine sediments from the North Occidental Coast of Baja California, Mexico (NOCBC) and their potential aromatic hydrocarbon catabolic pathways.
Materials and methods
During the Southern California Bight Oceanographic Campaign, sediment samples were collected in September 2018 from 33 coastal sites from the Tijuana-San Diego border to Punta Banda Cape, Ensenada (Mexico). The samples were analyzed for grain size, total PAHs, and organic carbon (OC) concentrations. Next, the bacterial communities were identified using Illumina high-throughput sequencing of 16S rRNA genes, and hydrocarbonoclastic function was inferred using PICRUSt2.
Results
According to Canadian and EPA guidelines for marine sediments, the total PAH concentration from the samples suggested a low pollution impact. Sequence analysis identified 27 phyla and 36 candidate divisions across the sampled sediments. The dominant phyla were Pseudomonadota, Bacteroidota, Planctomycetota, and Crenarchaeota. At the family level, the most prominent were Piscirickettsiaceae, OM60, Flavobacteriaceae, Pirellulaceae, and Cenarchaeaceae. The key genera were identified as Nitrosopumilus, Lutimonas, and Desulfococcus; nine Amplicon Sequence Variants (ASVs) represented the core microbiome across the sites, comprising about 7.68% of the total reads. The predictive functional analysis detected 47 principal pathways involved in hydrocarbon degradation, including catechol, protocatechuate, and aerobic toluene degradation routes.
Conclusions
Our data suggest the presence of hot spots for aromatic degradative pathways in those sampling sites near cities, where a significant proportion of aromatic hydrocarbon-degrading microorganisms may be present. This study represents the first census of the prokaryotic communities from marine sediments of NOCBC, which harbors diverse communities with hydrocarbonoclastic potential. These results could provide constructive guidelines on ecosystem management and pollution mitigation actions.
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Data availability
Sequence data have been deposited in the NCBI Sequence Read Archive (SRA), in the Bioproject PRJNA984743 and reference numbers SAMN35778037 to SAMN35778069.
References
Al-Mur BA (2019) Assessing the ecological risks from hydrocarbons in the marine coastal sediments of Jeddah. Red Sea Environ Monit Assess 191:180. https://doi.org/10.1016/10.1007/s10661-019-7262-1
Aldeguer-Riquelme B, Rubio-Portillo E, Álvarez-Rogel J, Giménez-Casalduero F, Otero XL, Belando MD, Bernardeau-Esteller J, García-Muñoz R, Forcada A, Ruiz JM, Santos F, Antón J (2022) Factors structuring microbial communities in highly impacted coastal marine sediments (Mar Menor lagoon, SE Spain). Front Microbiol 13:937683. https://doi.org/10.3389/fmicb.2022.937683
Andrews S (2010) FastQC: a quality control tool for high throughput sequence data. Available online at: http://www.bioinformatics.babraham.ac.uk/projects/fastqc. Accessed 15 Dec 2023
Arndt D, **a J, Liu Y et al (2012) METAGENassist: A comprehensive web server for comparative metagenomics. Nucleic Acids Res 40:W88–W95. https://doi.org/10.1093/nar/gks497
Arreola-Serrano AS, Mendoza-Espinosa LG, Hernández-Cruz A et al (2022) Quantifying the pollutant load into the Southern California Bight from Mexican sewage discharges from 2011 to 2020. Front Water. https://doi.org/10.3389/frwa.2022.993713
Barbera P, Kozlov AM, Czech L et al (2019) EPA-ng: Massively Parallel Evolutionary Placement of Genetic Sequences. Syst Biol 68:365–369. https://doi.org/10.1093/sysbio/syy054
Bolyen E, Rideout JR, Dillon MR et al (2019) Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nat Biotechnol 37:852–857. https://doi.org/10.1038/s41587-019-0209-9
Buchman MF (2008) NOAA Screening Quick Reference Tables (SQuiRTs), NOAA OR&R Report 08–1. Seattle WA, Office of Response and Restoration Division, National Oceanic and Atmospheric Administration. https://repository.library.noaa.gov/view/noaa/9327/noaa_9327_DS1.pdf. Accessed 2 Nov 2023
Burdige DJ (2007) Preservation of organic matter in marine sediments: controls, mechanisms, and an imbalance in sediment organic carbon budgets? Chem Rev 107:467–485. https://doi.org/10.1021/cr050347q
Callahan BJ, McMurdie PJ, Rosen MJ et al (2016) DADA2: High-resolution sample inference from Illumina amplicon data. Nat Methods 13:581–583. https://doi.org/10.1038/nmeth.3869
Caporaso JG, Lauber CL, Walters WA et al (2011) Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proc Natl Acad Sci USA 108:4516–4522. https://doi.org/10.1073/pnas.1000080107
Caspi R, Billington R, Ferrer L et al (2016) The MetaCyc database of metabolic pathways and enzymes and the BioCyc collection of pathway/genome databases. Nucleic Acids Res 44:D471–D480. https://doi.org/10.1093/nar/gkv1164
Chao A (1984) Nonparametric estimation of the number of classes in a population. Scand Stat Theory Appl 11:265–270
Chen Q, Fan J, Su J et al (2020) Spatial distribution characteristics of bacterial community structure and gene abundance in sediments of the Bohai Sea. Acta Oceanol 39:69–78. https://doi.org/10.1007/s13131-020-1554-8
Douglas GM, Maffei VJ, Zaneveld JR et al (2020) PICRUSt2 for prediction of metagenome functions. Nat Biotechnol 38:685–688. https://doi.org/10.1038/s41587-020-0548-6
de Piñon-Colin T, J, Rodriguez-Jimenez R, Pastrana-Corral MA et al (2018) Microplastics on sandy beaches of the Baja California Peninsula, Mexico. Mar Pollut Bull 131:63–71. https://doi.org/10.1016/j.marpolbul.2018.03.055
Dunlea AG, Scudder RP, Murray RW (2018) Marine Sediment. In: White WM (ed) Encyclopedia of Geochemistry. Encyclopedia of Earth Sciences Series. Springer, Cham. https://doi.org/10.1007/978-3-319-39312-4_105
Eddy SR (2011) Accelerated profile HMM searches. PLoS Comput Biol 7:e1002195. https://doi.org/10.1371/journal.pcbi.1002195
Escofet A, Espejel I (1999) Conservation and management-oriented ecological research in the coastal zone of Baja California, Mexico. J Coast Conserv 5:43–50. https://doi.org/10.1007/BF02802738
Fonseca A, Espinoza C, Nielsen LP et al (2022) Bacterial community of sediments under the Eastern Boundary Current System shows high microdiversity and a latitudinal spatial pattern. Front Microbiol 13:1016418. https://doi.org/10.3389/fmicb.2022.1016418
Franzo A, Auriemma R, Nasi F et al (2016) Benthic ecosystem functioning in the severely contaminated Mar Piccolo of Taranto (Ionian Sea, Italy): focus on heterotrophic pathways. Environ Sci Pollut Res 23:12645–12661. https://doi.org/10.1007/s11356-015-5339-0
Ge M, Wang X, Yang G et al (2021) Persistent organic pollutants (POPs) in deep-sea sediments of the tropical western Pacific Ocean. Chemosphere 277:130267. https://doi.org/10.1016/j.chemosphere.2021.130267
Ghosal D, Ghosh S, Dutta TK et al (2016) Current state of knowledge in microbial degradation of polycyclic aromatic hydrocarbons (PAH): A review. Front Microbiol 7:1369. https://doi.org/10.3389/fmicb.2016.01369
Guevara G, Castillo Lopez M, Alonso S et al (2019) New insights into the genome of Rhodococcus ruber strain Chol-4. BMC Genomics 20:332. https://doi.org/10.1186/s12864-019-5677-2
Hammer Ø, Hammer DAT, Ryan PD (2001) Past: Paleontological statistics software package for education and data analysis. Palaentol Electron 4:1–9
Heinrich L, Dietel J, Hupfer M (2022) Sulphate reduction determines the long-term effect of iron amendments on phosphorus retention in lake sediments. J Soils Sediments 22:316–333. https://doi.org/10.1007/s11368-021-03099-3
Hyland J, Balthis L, Karakassis I et al (2005) Organic carbon content of sediments as an indicator of stress in the marine benthos. Mar Ecol Prog Ser 295:91–103. https://doi.org/10.3354/meps295091
Jessen GL, Lichtschlag A, Ramette A et al (2017) Hypoxia causes preservation of labile organic matter and changes seafloor microbial community composition (Black Sea). Sci Adv 3:e1601897. https://doi.org/10.1126/sciadv.1601897
Jokanović S, Kajan K, Perović S et al (2021) Anthropogenic influence on the environmental health along Montenegro coast based on the bacterial and chemical characterization. Environ Pollut 271:116383. https://doi.org/10.1016/j.envpol.2020.116383
Kanehisa M, Goto S (2000) KEGG: Kyoto Encyclopedia of Genes and Genomes. Nucleic Acids Res 28:27–30. https://doi.org/10.1093/nar/28.1.27
Kim YO, Park S, Nam BH et al (2014) Description of Lutimonas halocynthiae sp. nov, isolated from a golden sea squirt (Halocynthia aurantium), reclassification of Aestuariicola saemankumensis as Lutimonas saemankumensis comb. nov. and emended description of the genus Lutimonas Int J Syst Evol Microbiol 64:1984–1990. https://doi.org/10.1099/ijs.0.059923-0
Kleindienst S, Herbst FA, Stagars M et al (2014) Diverse sulfate-reducing bacteria of the Desulfosarcina/Desulfococcus clade are the key alkane degraders at marine seeps. ISME J 8:2029–2044. https://doi.org/10.1038/ismej.2014.51
Kniemeyer O, Musat F, Sievert SM et al (2007) Anaerobic oxidation of short-chain hydrocarbons by marine sulphate-reducing bacteria. Nature 449:898–901. https://doi.org/10.1038/nature06200
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
Lalzar M, Zvi-Kedem T, Kroin Y, Martinez S, Tchernov D, Meron D (2023) Sediment microbiota as a proxy of environmental health: Discovering inter- and intrakingdom dynamics along the Eastern Mediterranean continental shelf. Microbiol Spectr 11:e0224222. https://doi.org/10.1128/spectrum.02242-22
Lee Y, Jeong HI, Jeong SE et al (2016) Zeaxanthinibacter aestuarii sp. nov., isolated from estuary sediment and emended description of the genus Zeaxanthinibacter Asker et al. 2007. Int J Syst Evol Microbiol 66:3264–3269. https://doi.org/10.1099/ijsem.0.001185
Li J, Li A, Li Y et al (2022) PICRUSt2 functionally predicts organic compounds degradation and sulfate reduction pathways in an acidogenic bioreactor. Front Environ Sci Eng 16:47. https://doi.org/10.1007/s11783-021-1481-8
Long ER, Macdonald DD, Smith SL et al (1995) Incidence of adverse effects within ranges of chemical concentrations in marine and estuarine sediments. Environ Management 19:81–97. https://doi.org/10.1007/BF02472006
Louca S, Doebeli M (2018) Efficient comparative phylogenetics on large trees. Bioinformatics 34:1053–1055. https://doi.org/10.1093/bioinformatics/btx701
Lozupone C, Lladser ME, Knights D et al (2011) UniFrac: An effective distance metric for microbial community comparison. ISME J 5:169–172. https://doi.org/10.1038/ismej.2010.133
Lu M, Luo X, Jiao JJ et al (2019) Nutrients and heavy metals mediate the distribution of microbial community in the marine sediments of the Bohai Sea. China Environ Pollut 255:113069. https://doi.org/10.1016/j.envpol.2019.113069
Macías-Zamora JV, Meléndez-Sánchez AL, Ramírez-Álvarez N et al (2014a) On the effects of the dispersant Corexit 9500© during the degradation process of n-alkanes and PAH in marine sediments. Environ Monit Assess 186:1051–1061. https://doi.org/10.1007/s10661-013-3438-2
Macías-Zamora JV, Mendoza-Vega E, Villaescusa-Celaya JA (2002) PAH composition of surface marine sediments: a comparison to potential local sources in Todos Santos Bay, B. C. Mexico Chemosphere 46:459–468. https://doi.org/10.1016/S0045-6535(01)00069-8
Macías-Zamora JV, Ramírez-Álvarez N, Hernández-Guzmán FA et al (2016) On the sources of PBDEs in coastal marine sediments off Baja California, Mexico. Sci Total Environ 571:59–66. https://doi.org/10.1016/j.scitotenv.2016.07.142
Macías-Zamora JV, Ramírez-Álvarez N, Sánchez-Osorio JL (2014b) A decadal trend study (1998–2008) of POPs in marine sediments at the south of the Southern California Bight. Sci Total Environ 491–492:205–211. https://doi.org/10.1016/j.scitotenv.2014.02.011
Marchant HK, Tegetmeyer HE, Ahmerkamp S et al (2018) Metabolic specialization of denitrifiers in permeable sediments controls N2O emissions. Environ Microbiol 20:4486–4502. https://doi.org/10.1111/1462-2920.14385
McDonald D, Price MN, Goodrich J et al (2012) An improved Greengenes taxonomy with explicit ranks for ecological and evolutionary analyses of bacteria and archaea. ISME J 6:610–618. https://doi.org/10.1038/ismej.2011.139
McMurdie PJ, Holmes S (2013) phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS ONE 8:e61217. https://doi.org/10.1371/journal.pone.0061217
Nakata H, Uehara K, Goto Y et al (2014) Polycyclic aromatic hydrocarbons in oysters and sediments from the Yatsushiro Sea, Japan: Comparison of potential risks among PAH, dioxins and dioxin-like compounds in benthic organisms. Ecotoxicol Environ Saf 99:61–68. https://doi.org/10.1016/j.ecoenv.2013.10.005
Navarrete-Euan H, Rodríguez-Escamilla Z, Pérez-Rueda E et al (2021) Comparing sediment microbiomes in contaminated and pristine wetlands along the coast of Yucatan. Microorganisms 9:887. https://doi.org/10.3390/microorganisms9040877
Pandolfo E, Barra Caracciolo A, Rolando L (2023) Recent Advances in Bacterial Degradation of Hydrocarbons. Water 15:375. https://doi.org/10.3390/w15020375
Partida-Gutiérrez DI, Villaescusa JA, Macías Zamora JV et al (2003) Persistent organic pollutants in sediment cores from the southern region of the Bight of the Californias. Cienc Mar 29:521–534. https://doi.org/10.7773/cm.v29i4.164
Pastrana-Corral MA, Wakida FT, Temores-Peña J et al (2017) Heavy metal pollution in the soil surrounding a thermal power plant in Playas de Rosarito. Mexico Environ Earth Sci 76:583. https://doi.org/10.1007/s12665-017-6928-7
Patel AB, Jain KR, Manvar T et al (2022) Enriched bacterial community efficiently degrade polycyclic aromatic hydrocarbons in soil ecosystem: Insights from a mesocosms study. Biochem Eng J 185:108516. https://doi.org/10.1016/j.bej.2022.108516
Patel AB, Shaikh S, Jain KR et al (2020) Polycyclic aromatic hydrocarbons: sources, toxicity, and remediation approaches. Front Microbiol. https://doi.org/10.3389/fmicb.2020.562813
Probandt D, Knittel K, Tegetmeyer HE, Ahmerkamp S, Holtappels M, Amann R (2017) Permeability shapes bacterial communities in sublittoral surface sediments. Environ Microbiol 19:1584–1599. https://doi.org/10.1111/1462-2920.13676
Qin W, Heal KR, Ramdasi R et al (2017) Nitrosopumilus maritimus gen. nov., sp. nov., Nitrosopumilus cobalaminigenes sp. nov., Nitrosopumilus oxyclinae sp. nov., and Nitrosopumilus ureiphilus sp. nov., four marine ammonia-oxidizing archaea of the phylum Thaumarchaeota. Int J Syst Evol Microbiol 67:5067–5079. https://doi.org/10.1099/ijsem.0.002416
Quintero-Nuñez M, Sanchez-Sanchez CC, Garcia-Cueto R et al (2014) Environmental impact of the Energía Costa Azul LNG terminal at Ensenada, B.C. México WIT Trans Ecol Environ 181:15–24. https://doi.org/10.2495/EID140021
Quero GM, Cassin D, Botter M et al (2015) Patterns of benthic bacterial diversity in coastal areas contaminated by heavy metals, polycyclic aromatic hydrocarbons (PAHs) and polychlorinated biphenyls (PCBs). Front Microbiol 6:1053. https://doi.org/10.3389/fmicb.2015.01053
Ramette A (2007) Multivariate analyses in microbial ecology. FEMS Microbiol Ecol 62:142–160. https://doi.org/10.1111/j.1574-6941.2007.00375.x
Reid A, Buckley M (2011) The Rare Biosphere. Ed. American Society for Microbiology. Available from: https://www.ncbi.nlm.nih.gov/books/NBK560451/. Accessed 15 Nov 2023
Reyes-Sosa MB, Apodaca-Hernández JE, Arena-Ortiz ML (2018) Bioprospecting for microbes with potential hydrocarbon remediation activity on the northwest coast of the Yucatan Peninsula, Mexico, using DNA sequencing. Sci Total Environ 642:1060–1074. https://doi.org/10.1016/j.scitotenv.2018.06.097
RStudio Team (2020). RStudio: Integrated Development for R. RStudio, PBC, Boston, MA. Available online at: http://www.rstudio.com/
Santoro AE, Casciotti KL (2011) Enrichment and characterization of ammonia-oxidizing archaea from the open ocean: Phylogeny, physiology and stable isotope fractionation. ISME J 5:1796–1808. https://doi.org/10.1038/ismej.2011.58
Shade A, Handelsman J (2012) Beyond the Venn diagram: the hunt for a core microbiome. Environ Microbiol 14:4–12. https://doi.org/10.1111/j.1462-2920.2011.02585.x
Shannon CE (1948) A mathematical theory of communication. Bell Syst Tech J 27:379–423. https://doi.org/10.1002/j.1538-7305.1948.tb01338.x
Silva-Jiménez H, Araujo-Palomares CL, Macías-Zamora JV et al (2018) Identification by MALDI-TOF MS of environmental bacteria with high potential to degrade pyrene. J Mex Chem Soc 62:214–225. https://doi.org/10.29356/jmcs.v62i2.411
Simpson E (1949) Measurement of Diversity. Nature 163:688. https://doi.org/10.1038/163688a0
Suárez-Moo P, Lamelas A, Garcia-Bautista I et al (2020) Characterization of sediment microbial communities at two sites with low hydrocarbon pollution in the southeast Gulf of Mexico. PeerJ 8(8):e10339. https://doi.org/10.7717/peerj.10339
Terrill E, Peck S, Hazard L et al (2006) The Southern California Coastal Ocean Observing System. In: OCEANS 2006, Boston, MA, USA, pp 1–8. https://doi.org/10.1109/OCEANS.2006.306877
Ul-Hasan S, Bowers RM, Figueroa-Montiel A et al (2019) Community ecology across bacteria, archaea and microbial eukaryotes in the sediment and seawater of coastal Puerto Nuevo. Baja California Plos One 14:e0212355. https://doi.org/10.1371/journal.pone.0212355
Vera A, Wilson FP, Cupples AM (2022) Predicted functional genes for the biodegradation of xenobiotics in groundwater and sediment at two contaminated naval sites. Appl Microbiol Biotechnol 106:835–853. https://doi.org/10.1007/s00253-021-11756-3
Villegas-Jiménez A, Macías-Zamora JV, Villaescusa-Celaya JA (1996) Aliphatic and polycyclic aromatic hydrocarbons in surficial sediments of Bahía de Todos Santos, B. C. México Hidrobiológica 6:25–32
Wöhlbrand L, Jacob JH, Kube M et al (2013) Complete genome, catabolic sub-proteomes and key-metabolites of Desulfobacula toluolica Tol2, a marine, aromatic compound-degrading, sulfate-reducing bacterium. Environ Microbiol 15:1334–1355. https://doi.org/10.1111/j.1462-2920.2012.02885.x
Wu Y, Jiang B, Zou Y et al (2022) Influence of bacterial community diversity, functionality, and soil factors on polycyclic aromatic hydrocarbons under various vegetation types in mangrove wetlands. Environ Pollut 1(308):119622. https://doi.org/10.1016/j.envpol.2022.119622
Ye Q, Wu Y, Zhu Z et al (2016) Bacterial diversity in the surface sediments of the hypoxic zona near the Changjiang Estuary and in the East China Sea. Microbiology Open 5:323–339. https://doi.org/10.1002/mbo3.330
Ye Y, Doak TG (2009) A parsimony approach to biological pathway reconstruction/inference for genomes and metagenomes. PLoS Comput Biol 5:e1000465. https://doi.org/10.1371/journal.pcbi.1000465
Zhang C, Meckenstock RU, Weng S et al (2021) Marine sediments harbor diverse archaea and bacteria with the potential for anaerobic hydrocarbon degradation via fumarate addition. FEMS Microbiol Ecol 97:fiab045. https://doi.org/10.1093/femsec/fiab045
Acknowledgements
We would like to acknowledge the help of the “Alguita” catamaran and Captain Charles Moore for his support in collecting sediment samples.
Funding
This work was supported by the project IIO-UABC 22nd internal call of the Universidad Autónoma de Baja California (Project UABC 646). Salvador Embarcadero-Jiménez and Ileana Sarahi Ramos received postdoctoral -aided and master fellowship support from CONACyT "Consejo Nacional de Ciencia y Tecnología" (now CONAHCyT), respectively.
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Ileana Sarahi Ramos-Mendoza and Salvador Embarcadero-Jiménez: Formal Analysis, Investigation, Visualization, Writing of the original draft. Andrea Fernanda Barrios-Navarro, Diana Camila Ledezma-González. and Brianda Jannyn Valenzuela-Suárez: Formal Analysis and Investigation. Asunción Lago-Lestón: Investigation, Resources, Writing - Review & Editing. Nancy Ramírez-Álvarez: Investigation, Review & Resources. Hortencia Silva-Jiménez: Conceptualization, Resources, Supervision, Funding acquisition, Writing - Review & Editing.
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Ramos-Mendoza, I.S., Embarcadero-Jiménez, S., Barrios-Navarro, A.F. et al. Prokaryotic community structure and predicted metabolism associated with hydrocarbon degradation in marine sediments from the Northwest Coast of Baja California, Mexico. J Soils Sediments (2024). https://doi.org/10.1007/s11368-024-03822-w
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DOI: https://doi.org/10.1007/s11368-024-03822-w