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

Shawn M Doyle; Genmei Lin; Maya Morales-McDevitt; Terry L Wade; Antonietta Quigg; Jason B Sylvan

doi:10.1128/mSystems.00668-20

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

mSystems. 2020 Aug 25;5(4):e00668-20. doi: 10.1128/mSystems.00668-20.

Authors

Shawn M Doyle¹, Genmei Lin², Maya Morales-McDevitt³, Terry L Wade^{4

5}, Antonietta Quigg^{4

6}, Jason B Sylvan¹

Affiliations

¹ Department of Oceanography, Texas A&M University, College Station, Texas, USA shawndoyle@tamu.edu jasonsylvan@tamu.edu.
² School of Marine Sciences, Sun Yat-sen University, Zhuhai, China.
³ Graduate School of Oceanography, University of Rhode Island, Narragansett, Rhode Island, USA.
⁴ Department of Oceanography, Texas A&M University, College Station, Texas, USA.
⁵ Geochemical and Environmental Research Group, Texas A&M University, College Station, Texas, USA.
⁶ Department of Marine Biology, Texas A&M University at Galveston, Galveston, Texas, USA.

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.

Keywords: dispersants; ecotones; metatranscriptomics; oil spills.