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Dramatic shifts in benthic microbial eukaryote communities following the Deepwater Horizon oil spill.

Bik HM, Halanych KM, Sharma J, Thomas WK - PLoS ONE (2012)

Bottom Line: Post-spill fungal taxa exhibit low richness and are characterized by an abundance of known hydrocarbon-degrading genera, compared to prior communities that contained smaller and more diverse fungal assemblages.Comparative taxonomic data from nematodes further suggests drastic impacts; while pre-spill samples exhibit high richness and evenness of genera, post-spill communities contain mainly predatory and scavenger taxa alongside an abundance of juveniles.Based on this community analysis, our data suggest considerable (hidden) initial impacts across Gulf beaches may be ongoing, despite the disappearance of visible surface oil in the region.

View Article: PubMed Central - PubMed

Affiliation: Hubbard Center for Genome Studies, University of New Hampshire, Durham, New Hampshire, United States of America. holly.bik@gmail.com

ABSTRACT
Benthic habitats harbour a significant (yet unexplored) diversity of microscopic eukaryote taxa, including metazoan phyla, protists, algae and fungi. These groups are thought to underpin ecosystem functioning across diverse marine environments. Coastal marine habitats in the Gulf of Mexico experienced visible, heavy impacts following the Deepwater Horizon oil spill in 2010, yet our scant knowledge of prior eukaryotic biodiversity has precluded a thorough assessment of this disturbance. Using a marker gene and morphological approach, we present an intensive evaluation of microbial eukaryote communities prior to and following oiling around heavily impacted shorelines. Our results show significant changes in community structure, with pre-spill assemblages of diverse Metazoa giving way to dominant fungal communities in post-spill sediments. Post-spill fungal taxa exhibit low richness and are characterized by an abundance of known hydrocarbon-degrading genera, compared to prior communities that contained smaller and more diverse fungal assemblages. Comparative taxonomic data from nematodes further suggests drastic impacts; while pre-spill samples exhibit high richness and evenness of genera, post-spill communities contain mainly predatory and scavenger taxa alongside an abundance of juveniles. Based on this community analysis, our data suggest considerable (hidden) initial impacts across Gulf beaches may be ongoing, despite the disappearance of visible surface oil in the region.

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Bray-curtis similarity of morphologically identified nematode communities.Group average cluster analysis based on faunal resemblance; Bray-Curtis similarity of nematode genera calculated from pre-spill and post spill samples based on presence/absence of genera.
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pone-0038550-g003: Bray-curtis similarity of morphologically identified nematode communities.Group average cluster analysis based on faunal resemblance; Bray-Curtis similarity of nematode genera calculated from pre-spill and post spill samples based on presence/absence of genera.

Mentions: Marker gene datasets indicate a substantial shift in eukaryote communities between pre-spill and post-spill samples. Pre-spill sediments contain a high diversity of metazoan phyla, with the majority of sites showing an expected dominance of nematode taxa. In contrast, most post-spill sites are overwhelmingly dominated by fungi and show corresponding decreases in the number of metazoan taxa recovered. The observed patterns (Figure 1) were consistent regardless of the computational approach used to process data; community patterns were repeatedly recovered across a range of OTU clustering cutoffs in multiple pipelines, withstood denoising [4], and were not affected by three independent approaches for chimera checking/removal. Phylogenetically-informed beta diversity analyses (carried out using the UniFrac distance metric [5] implemented in the QIIME pipeline [6]) further support a distinction between pre-spill and post-spill eukaryote communities (Figure 2). None of our community structure analyses recovered a close relationship between paired pre- and post-spill replicates; instead, post-spill sites formed distinct groupings in both Principal Coordinate Analysis (PCoA) and Jackknife Cluster analysis. PCoA separated pre-spill sites across axes indicating diverse and divergent community assemblages inhabiting these beaches. In contrast, most post-spill sites converged into a singular cluster, driven by a common set of putatively oil-tolerant eukaryotes that appear to subsequently dominate affected sites. Our parallel morphological approach confirms a significant change in nematode assemblages. Pre-spill samples exhibited a high species richness and overall evenness in types of feeding strategies represented by the genera present, whereas post-spill samples showed significantly lower nematode richness, a bias towards predatory species and scavengers, and resident populations showing atypical abundances of juvenile stages. Based on presence/absence of morphologically identified genera, Bray-Curtis similarity analyses further supported similar community assemblages at post-spill sites (Figure 3). Lowered nematode abundances and similar taxonomic biases have been previously documented following hydrocarbon contamination in marine habitats [7], supporting altered functional roles within microbial eukaryote communities following oil exposure. In addition, some predatory nematode species are known for facultative utilization of alternate food sources [8] including direct uptake of dissolved carbon. This ability may confer a competitive advantage to opportunistic nematode species that are able to thrive by ingesting fungal prey or environmental carbon in oil-affected sediments.


Dramatic shifts in benthic microbial eukaryote communities following the Deepwater Horizon oil spill.

Bik HM, Halanych KM, Sharma J, Thomas WK - PLoS ONE (2012)

Bray-curtis similarity of morphologically identified nematode communities.Group average cluster analysis based on faunal resemblance; Bray-Curtis similarity of nematode genera calculated from pre-spill and post spill samples based on presence/absence of genera.
© Copyright Policy
Related In: Results  -  Collection

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getmorefigures.php?uid=PMC3368851&req=5

pone-0038550-g003: Bray-curtis similarity of morphologically identified nematode communities.Group average cluster analysis based on faunal resemblance; Bray-Curtis similarity of nematode genera calculated from pre-spill and post spill samples based on presence/absence of genera.
Mentions: Marker gene datasets indicate a substantial shift in eukaryote communities between pre-spill and post-spill samples. Pre-spill sediments contain a high diversity of metazoan phyla, with the majority of sites showing an expected dominance of nematode taxa. In contrast, most post-spill sites are overwhelmingly dominated by fungi and show corresponding decreases in the number of metazoan taxa recovered. The observed patterns (Figure 1) were consistent regardless of the computational approach used to process data; community patterns were repeatedly recovered across a range of OTU clustering cutoffs in multiple pipelines, withstood denoising [4], and were not affected by three independent approaches for chimera checking/removal. Phylogenetically-informed beta diversity analyses (carried out using the UniFrac distance metric [5] implemented in the QIIME pipeline [6]) further support a distinction between pre-spill and post-spill eukaryote communities (Figure 2). None of our community structure analyses recovered a close relationship between paired pre- and post-spill replicates; instead, post-spill sites formed distinct groupings in both Principal Coordinate Analysis (PCoA) and Jackknife Cluster analysis. PCoA separated pre-spill sites across axes indicating diverse and divergent community assemblages inhabiting these beaches. In contrast, most post-spill sites converged into a singular cluster, driven by a common set of putatively oil-tolerant eukaryotes that appear to subsequently dominate affected sites. Our parallel morphological approach confirms a significant change in nematode assemblages. Pre-spill samples exhibited a high species richness and overall evenness in types of feeding strategies represented by the genera present, whereas post-spill samples showed significantly lower nematode richness, a bias towards predatory species and scavengers, and resident populations showing atypical abundances of juvenile stages. Based on presence/absence of morphologically identified genera, Bray-Curtis similarity analyses further supported similar community assemblages at post-spill sites (Figure 3). Lowered nematode abundances and similar taxonomic biases have been previously documented following hydrocarbon contamination in marine habitats [7], supporting altered functional roles within microbial eukaryote communities following oil exposure. In addition, some predatory nematode species are known for facultative utilization of alternate food sources [8] including direct uptake of dissolved carbon. This ability may confer a competitive advantage to opportunistic nematode species that are able to thrive by ingesting fungal prey or environmental carbon in oil-affected sediments.

Bottom Line: Post-spill fungal taxa exhibit low richness and are characterized by an abundance of known hydrocarbon-degrading genera, compared to prior communities that contained smaller and more diverse fungal assemblages.Comparative taxonomic data from nematodes further suggests drastic impacts; while pre-spill samples exhibit high richness and evenness of genera, post-spill communities contain mainly predatory and scavenger taxa alongside an abundance of juveniles.Based on this community analysis, our data suggest considerable (hidden) initial impacts across Gulf beaches may be ongoing, despite the disappearance of visible surface oil in the region.

View Article: PubMed Central - PubMed

Affiliation: Hubbard Center for Genome Studies, University of New Hampshire, Durham, New Hampshire, United States of America. holly.bik@gmail.com

ABSTRACT
Benthic habitats harbour a significant (yet unexplored) diversity of microscopic eukaryote taxa, including metazoan phyla, protists, algae and fungi. These groups are thought to underpin ecosystem functioning across diverse marine environments. Coastal marine habitats in the Gulf of Mexico experienced visible, heavy impacts following the Deepwater Horizon oil spill in 2010, yet our scant knowledge of prior eukaryotic biodiversity has precluded a thorough assessment of this disturbance. Using a marker gene and morphological approach, we present an intensive evaluation of microbial eukaryote communities prior to and following oiling around heavily impacted shorelines. Our results show significant changes in community structure, with pre-spill assemblages of diverse Metazoa giving way to dominant fungal communities in post-spill sediments. Post-spill fungal taxa exhibit low richness and are characterized by an abundance of known hydrocarbon-degrading genera, compared to prior communities that contained smaller and more diverse fungal assemblages. Comparative taxonomic data from nematodes further suggests drastic impacts; while pre-spill samples exhibit high richness and evenness of genera, post-spill communities contain mainly predatory and scavenger taxa alongside an abundance of juveniles. Based on this community analysis, our data suggest considerable (hidden) initial impacts across Gulf beaches may be ongoing, despite the disappearance of visible surface oil in the region.

Show MeSH
Related in: MedlinePlus