Distinct microbial community along the chronic oil pollution continuum of the Persian Gulf converge with oil spill accidents

Abstract

The Persian Gulf, hosting ca. 48% of the world's oil reserves, has been chronically exposed to natural oil seepage. Oil spill studies show a shift in microbial community composition in response to oil pollution; however, the influence of chronic oil exposure on the microbial community remains unknown. We performed genome-resolved comparative analyses of the water and sediment samples along Persian Gulf's pollution continuum (Strait of Hormuz, Asalouyeh, and Khark Island). Continuous exposure to trace amounts of pollution primed the intrinsic and rare marine oil-degrading microbes such as Oceanospirillales, Flavobacteriales, Alteromonadales, and Rhodobacterales to bloom in response to oil pollution in Asalouyeh and Khark samples. Comparative analysis of the Persian Gulf samples with 106 oil-polluted marine samples reveals that the hydrocarbon type, exposure time, and sediment depth are the main determinants of microbial response to pollution. High aliphatic content of the pollution enriched for Oceanospirillales, Alteromonadales, and Pseudomonadales whereas, Alteromonadales, Cellvibrionales, Flavobacteriales, and Rhodobacterales dominate polyaromatic polluted samples. In chronic exposure and oil spill events, the community composition converges towards higher dominance of oil-degrading constituents while promoting the division of labor for successful bioremediation.

Figure 1

Geographical location of the sampling sites along the pollution continuum of the Persian Gulf. Hormuz sampling point is located close to the Persian Gulf’s marine input water, Asalouyeh sampling point is mainly exposed to aromatic oil contaminants and Khark sampling point is exposed to pollution with different crude oil derivatives. Sampling locations are marked with red squares. Figure was plotted using the open-source maps of the “rnaturalearth” library in R.

Figure 2

Prokaryotic community composition of the Persian Gulf water (A) and sediment (B) samples according to the abundance of 16S rDNA reads in unassembled metagenomes. Column names are microbial taxa at the order level. For some taxa with lower frequency, the sum of orders is displayed in their corresponding higher taxonomic level. There are a total number of 28 and 48 taxa for water and sediment samples, respectively by which samples are compared. Rows are the name of samples. Dendrograms represent the clustering of columns based on Pearson correlation. Figure was plotted using “circlize” and “ComplexHeatmap” packages in R.

Figure 3

The abundance of unassembled 16S rDNA reads from unassembled metagenomes of different oil-polluted water samples (41). Row names are microbial taxa at the order level. For taxa with lower frequency, the higher taxonomic level is shown (47 taxa in total). The right-hand dendrogram represents the clustering of rows based on the Pearson correlation. Columns are the name of water samples. Samples are clustered based on Pearson correlation and the color scale on the top left represents the row Z-score. Figure was plotted using “circlize” and “ComplexHeatmap” packages in R.

Figure 4

Non-metric multidimensional scaling (NMDS) of the Persian Gulf water and sediment metagenomes along with oil-polluted marine water and sediment metagenomes based on Bray–Curtis dissimilarity of the abundance of 16S rDNA reads in unassembled metagenomes at the order level. Samples with different geographical locations are shown in different colors. PG water and sediment samples are shown in red. Water and sediment samples are displayed by triangle and square shapes, respectively. Figure was plotted using “vegan” library in R.

Figure 5

The abundance of unassembled 16S rDNA reads from unassembled metagenomes of different oil-polluted sediment samples (65). Row names are microbial taxa at the order level. For taxa with lower frequency, the higher taxonomic level is shown (77 taxa in total). The right-hand dendrogram represents the clustering of rows based on the Pearson correlation. Columns are the name of sediment samples. Samples are clustered based on Pearson correlation and the color scale on the top left represents the row Z-score. Figure was plotted using “circlize” and “ComplexHeatmap” packages in R.

Figure 6

Hydrocarbon degrading enzymes present in recovered MAGs from the PG water and sediment metagenomes. Row names represent the taxonomy of recovered MAGs and their completeness is provided as a bar plot on the right side. The color indicates the MAG origin. The size of dots indicates the presence or absence of each enzyme in each recovered MAG. Columns indicate the type of hydrocarbon and in the parenthesis is the name of the enzyme hydrolyzing this compound followed by its corresponding KEGG orthologous accession number. Figure was plotted using “reshape2” and “ggplot2” packages in R.

Figure 7

The microbial community dynamics of the Persian Gulf water and sediment samples in response to oil pollution and their degradation potential. (A) Overview based on16S rDNA abundance. Hormuz Island was considered as a control location with the least impact from oil pollution. Taxa written in the blue frame are prevalent marine representatives present in HW. Microbial taxa in the Purple frame are mainly detected in OMZ areas and are also present in HW. Samples collected from Asalouyeh province are exposed to potential pollution caused by Gas field wastes. High oil trafficking, oil exploration and extraction, and natural oil seepage are the primary potential pollution sources in Khark Island. The possible pollutant types are shown in gray; however, the hydrocarbon pollution was below the detection limit in collected water samples. Black circles represent microorganisms that are involved in HC degradation in water samples from Asalouyeh and Khark Island. Microbes involved in sulfur and nitrogen cycle are shown in yellow and Red circles, respectively. HS and AS had similar silt and sand-sized sediments with HC below the detection limit. KhS had gravel-sized particles and showed the highest oil pollution shown in white. (B) MAGs containing key enzymes for degradation of aliphatic and cycloalkane compounds under aerobic conditions. (C) MAGs containing key enzymes for degradation of aromatic compounds under aerobic conditions. PG MAGs did not have Key enzymes for hydrocarbon degradation under anaerobic conditions therefore, it is not shown. Red circles in B and C panels represent key enzymes involved in the degradation. The name of MAGs containing mentioned enzymes are written in rectangles. The MAGs are colored based on the samples they have been recovered from and the legend is shown in the lower right corner. Figure has been created with “BioRender.com”.