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Niche Partitioning between Coastal and Offshore Shelf Waters Results in Differential Expression of Alkane and Polycyclic Aromatic Hydrocarbon Catabolic Pathways.

ABSTRACT: Marine oil spills can impact both coastal and offshore marine environments, but little information is available on how the microbial response to oil and dispersants might differ between these biomes. Here, we describe the compositional and functional response of microbial communities to different concentrations of oil and chemically dispersed oil in coastal and offshore surface waters from the Texas-Louisiana continental shelf. Using a combination of analytical chemistry and 16S rRNA amplicon and metatranscriptomic sequencing, we provide a broad, comparative overview of the ecological response of hydrocarbon-degrading bacteria and their expression of hydrocarbon-degrading genes in marine surface waters over time between two oceanic biomes. We found evidence for the existence of different ecotypes of several commonly described hydrocarbon-degrading bacterial taxa which behaved differentially in coastal and offshore shelf waters despite being exposed to similar concentrations of oil, dispersants, and nutrients. This resulted in the differential expression of catabolic pathways for n-alkanes and polycyclic aromatic hydrocarbons (PAHs)-the two major categories of compounds found in crude oil-with preferential expression of n-alkane degradation genes in coastal waters while offshore microbial communities trended more toward the expression of PAH degradation genes. This was unexpected as it contrasts with the generally held view that n-alkanes, being more labile, are attacked before the more refractory PAHs. Collectively, our results provide new insights into the existence and potential consequences of niche partitioning of hydrocarbon-degrading taxa between neighboring marine environments.IMPORTANCE In the wake of the Deepwater Horizon oil spill, the taxonomic response of marine microbial communities to oil and dispersants has been extensively studied. However, relatively few studies on the functional response of these microbial communities have been reported, especially in a longitudinal fashion. Moreover, despite the fact that marine oil spills typically impact thousands of square kilometers of both coastal and offshore marine environments, little information is available on how the microbial response to oil and dispersants might differ between these biomes. The results of this study help fill this critical knowledge gap and provide valuable insight into how oil spill response efforts, such as chemically dispersing oil, may have differing effects in neighboring coastal and offshore marine environments.

SUBMITTER: Doyle SM

PROVIDER: S-EPMC7449609 | biostudies-literature | 2020 Aug

REPOSITORIES: biostudies-literature

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Niche Partitioning between Coastal and Offshore Shelf Waters Results in Differential Expression of Alkane and Polycyclic Aromatic Hydrocarbon Catabolic Pathways.

Doyle Shawn M SM Lin Genmei G Morales-McDevitt Maya M Wade Terry L TL Quigg Antonietta A Sylvan Jason B JB

mSystems 20200825 4

Marine oil spills can impact both coastal and offshore marine environments, but little information is available on how the microbial response to oil and dispersants might differ between these biomes. Here, we describe the compositional and functional response of microbial communities to different concentrations of oil and chemically dispersed oil in coastal and offshore surface waters from the Texas-Louisiana continental shelf. Using a combination of analytical chemistry and 16S rRNA amplicon an ...[more]

PMID: 32843540

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Project description:BackgroundDinoflagellates are a ubiquitous and ecologically important component of marine phytoplankton communities, with particularly notable species including those associated with harmful algal blooms (HABs) and those that bioluminesce. High-throughput sequencing offers a novel approach compared to traditional microscopy for determining species assemblages and distributions of dinoflagellates, which are poorly known especially in Australian waters.ResultsWe assessed the composition of dinoflagellate assemblages in two Australian locations: coastal temperate Port Phillip Bay and offshore tropical waters of Davies Reef (Great Barrier Reef). These locations differ in certain environmental parameters reflecting latitude as well as possible anthropogenic influences. Molecular taxonomic assessment revealed more species than traditional microscopy, and it showed statistically significant differences in dinoflagellate assemblages between locations. Bioluminescent species and known associates of HABs were present at both sites. Dinoflagellates in both areas were mainly represented by the order Gymnodiniales (66%-82% of total sequence reads). In the warm waters of Davies Reef, Gymnodiniales were equally represented by the two superclades, Gymnodiniales sensu stricto (33%) and Gyrodinium (34%). In contrast, in cooler waters of Port Phillip Bay, Gymnodiniales was mainly represented by Gyrodinium (82%). In both locations, bioluminescent dinoflagellates represented up to 0.24% of the total sequence reads, with Protoperidinium the most abundant genus. HAB-related species, mainly represented by Gyrodinium, were more abundant in Port Phillip Bay (up to 47%) than at Davies Reef (28%), potentially reflecting anthropogenic influence from highly populated and industrial areas surrounding the bay. The entire assemblage of dinoflagellates, as well as the subsets of HAB and bioluminescent species, were strongly correlated with water quality parameters (R2 = 0.56-0.92). Significant predictors differed between the subsets: HAB assemblages were explained by salinity, temperature, dissolved oxygen, and total dissolved solids; whereas, bioluminescent assemblages were explained only by salinity and dissolved oxygen, and had greater variability.ConclusionHigh-throughput sequencing and genotyping revealed greater diversity of dinoflagellate assemblages than previously known in both subtropical and temperate Australian waters. Significant correlations of assemblage structure with environmental variables suggest the potential for explaining the distribution and composition of both HAB species and bioluminescent species.

Project description:Microbial communities in marine oxygen deficient zones (ODZs) are responsible for up to half of marine N loss through conversion of nutrients to N2O and N2. This N loss is accomplished by a consortium of diverse microbes, many of which remain uncultured. Here, we characterize genes for all steps in the anoxic N cycle in metagenomes from the water column and >30 μm particles from the Eastern Tropical North Pacific (ETNP) ODZ. We use an approach that allows for both phylogenetic identification and semi-quantitative assessment of gene abundances from individual organisms, and place these results in context of chemical measurements and rate data from the same location. Denitrification genes were enriched in >30 μm particles, even in the oxycline, while anammox bacteria were not abundant on particles. Many steps in denitrification were encoded by multiple phylotypes with different distributions. Notably three N2O reductases (nosZ), each with no cultured relative, inhabited distinct niches; one was free-living, one dominant on particles and one had a C terminal extension found in autotrophic S-oxidizing bacteria. At some depths >30% of the community possessed nitrite reductase nirK. A nirK OTU linked to SAR11 explained much of this abundance. The only bacterial gene found for NO reduction to N2O in the ODZ was a form of qnorB related to the previously postulated "nitric oxide dismutase," hypothesized to produce N2 directly while oxidizing methane. However, similar qnorB-like genes are also found in the published genomes of many bacteria that do not oxidize methane, and here the qnorB-like genes did not correlate with the presence of methane oxidation genes. Correlations with N2O concentrations indicate that these qnorB-like genes likely facilitate NO reduction to N2O in the ODZ. In the oxycline, qnorB-like genes were not detected in the water column, and estimated N2O production rates from ammonia oxidation were insufficient to support the observed oxycline N2O maximum. However, both qnorB-like and nosZ genes were present within particles in the oxycline, suggesting a particulate source of N2O and N2. Together, our analyses provide a holistic view of the diverse players in the low oxygen nitrogen cycle.

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Dataset Information

Niche Partitioning between Coastal and Offshore Shelf Waters Results in Differential Expression of Alkane and Polycyclic Aromatic Hydrocarbon Catabolic Pathways.

Publications

Niche Partitioning between Coastal and Offshore Shelf Waters Results in Differential Expression of Alkane and Polycyclic Aromatic Hydrocarbon Catabolic Pathways.

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