The impact of dissolved inorganic nitrogen and phosphorous on responses of microbial plankton to the Texas City “Y” oil spill in Galveston Bay, Texas (USA)

https://doi.org/10.1016/j.marpolbul.2017.05.033Get rights and content

Highlights

  • Functionally different microbial groups respond differently to oil and nutrients.

  • Nutrient amendments increased microbial abundance corresponding to decreased PAHs.

  • Nutrient stimulation of microbial bioremediation in estuaries may be successful.

Abstract

Ongoing bioremediation research seeks to promote naturally occurring microbial polycyclic aromatic hydrocarbon (PAH) degradation during and after oil spill events. However, complex relationships among functionally different microbial groups, nutrients and PAHs remain unconstrained. We conducted a surface water survey and corresponding nutrient amendment bioassays following the Texas City “Y” oil spill in Galveston Bay, Texas. Resident microbial groups, defined as either heterotrophic or autotrophic were enumerated by flow cytometry. Heterotrophic abundance was increased by oil regardless of nutrient concentrations. Contrastingly, autotrophic abundance was inhibited by oil, but this reaction was less severe when nutrient concentrations were higher. Several PAH compounds were reduced in nutrient amended treatments relative to controls suggesting nutrient enhanced microbial PAH processing. These findings provide a first-look at nutrient limitation during microbial oil processing in Galveston Bay, an important step in understanding if nutrient additions would be a useful bioremediation strategy in this and other estuarine systems.

Introduction

For many years anthropogenic releases of petrochemicals into marine environments have been documented (Jernelöv, 2010). Several of the environmental, human health and economic consequences have been recently reviewed (D'Andrea and Reddy, 2014, Ventikos and Sotiropoulos, 2014). Oil spills are recognized to have very complex effects, and there is a need for continued research to improve future mitigation strategies (Jernelöv, 2010). Estuarine waterways frequently host petroleum transportation vessels that release oil during routine processes (e.g. tank cleaning, transfer of contents, engine maintenance) or, more noticeably, during accidents (Houston Advanced Research Houston Advanced Research Center, 2014, Jernelöv, 2010, Kennish, 2002). The highly developed and populated surroundings of many estuaries also makes them vulnerable to land sourced run-off of oil compounds (Jernelöv, 2010, Kennish, 2002, Othman et al., 2012). Many of the compounds found in oil, including but not limited to polycyclic aromatic hydrocarbons (PAHs), can be toxic or cause permanent changes in marine organisms. Not surprisingly, oil is predicted to be one of the most detrimental sources of anthropogenic pollution to estuaries (Kennish, 2002).

Microorganisms including fungi, bacteria, cyanobacteria and phytoplankton are capable of degrading hydrocarbons (Bacosa et al., 2015a, Cerniglia, 1992, Doyle et al., 2008) and some use PAHs as carbon source for growth and production (Doyle et al., 2008, Jeon and Madsen, 2013, Vila et al., 2015). Typically, low-molecular weight compounds such as benzene, naphthalene or anthracene are preferentially degraded (Bacosa et al., 2010, Doyle et al., 2008, Vila et al., 2015), but there is also evidence of high-molecular weight, more toxic, PAH compounds such as pyrene and fluoranthene being utilized by microbes in culture and the environment (Bacosa and Inoue, 2015, Kanaly and Harayama, 2010). Complex and complementary consortia can develop after spills such that certain populations will consume specific PAH compounds, deriving degradation products that a subsequent population will utilize (Vila et al., 2015). Similar findings have been reported for estuarine microbial assemblages during mesocosm experiments (Gilde and Pinckney, 2012, González et al., 2009, Lekunberri et al., 2010, Ortmann et al., 2012, Ortmann and Lu, 2015) but these types of studies have not yet been conducted in Galveston Bay (Texas, USA) despite the heavy influence of petrochemical industries in the region.

The potential for diverse microbial degradation processes to reduce contamination makes microbes valuable candidates for bioremediation after oil spills but success is dependent on the composition of the oil and the concurrent environmental conditions during the spill (Doyle et al., 2008, Ortmann and Lu, 2015, Sheppard et al., 2014). In particular, if the in situ microbial community is nutrient limited, the addition of nutrients can potentially stimulate greater biological degradation of hydrocarbons e.g. (Atlas and Bartha, 1972, Edwards et al., 2011, Head et al., 2006, Jean et al., 2008, Ron and Rosenberg, 2014) underscoring the importance of nutrient availability during oil spill events. It is estimated that 150 g of nitrogen and 30 g of phosphorous are required to convert 1 kg of hydrocarbons to cell material (Ron and Rosenberg, 2014). Consequently, the addition of inorganic nutrients has been suggested and utilized to stimulate bioremediation in different marine environments (Atlas and Bartha, 1972, Head et al., 2006, Sauret et al., 2015). In Galveston Bay, spatiotemporal co-limitation of microbial plankton and microalgae occurs and is related to interacting physicochemical factors including temperature, carbon, nitrogen and phosphorous availability (Dorado et al., 2015, Pinckney, 2006, Shepard, 2015).

On March 22, 2014, a collision between shipping vessels resulted in the discharge of 6.4 × 105 L of marine fuel oil (RMG-380) into Galveston Bay (Fig. 1). This event was henceforth known as the Texas City “Y” oil spill (Walpert et al., 2014, Yin et al., 2015). It was found that the proximity of this spill to land reduced the time for abiotic weathering processes to occur (e.g. photodegradation, dissolution, evaporation e.g., (Shankar et al., 2015)) because a characterization of the oil that rapidly accumulated on nearby beaches had high concentrations of total PAHs (Yin et al., 2015). These were primarily dominated by compounds including alkylated phenanthrenes, known to be toxic to marine organisms, and naphthalenes that are considered low molecular weight and highly volatile (Atlas, 1979, Yin et al., 2015). While weather conditions and currents quickly moved the bulk of the spilled oil out of the bay and into the Gulf of Mexico (Walpert et al., 2014), slicks (Fig. 1B) and tar balls (Bacosa et al., 2016) were visually present surrounding the spill site for several days, during which time oil compounds were presumably interacting with resident microbial communities in the water.

The purpose of this study was to evaluate changes in abundance of resident nano- and pico-plankton (2–20 μm) microbial groups using flow cytometry and bioassays in order to assess how nutrient availability may have influenced their respective responses to the spilled oil. Bioassay incubations reduce the effects of physical dispersion of contaminating oil allowing for statistical comparisons between oiled and un-oiled treatments with naturally occurring microbial assemblages. We hypothesized that heterotrophic bacteria would increase in total abundance, utilizing PAHs as a source of carbon and energy and that response would be intensified in the presence of nutrients. At the same time, the abundance of autotrophic microorganisms within the community would be repressed by exposure to oil, because of toxic effects and competition with bacteria for nutrients. Providing information on the relationships between microbial groups and PAH degradation can help determine if nutrient addition bioremediation strategies would be useful.

Section snippets

Study location

Galveston Bay (Fig. 1A), the seventh largest estuary in the United States (29°34 N, 94°56 W), is an economically and ecologically important estuary along the northern coast of the Gulf of Mexico (Gonzalez and Lester, 2011; Houston Advanced Research Center, 2014). Oil spills in Galveston Bay are typically small in volume, averaging ~ 100 gal per spill, with the majority of spills consisting of < 1 gal (Figs. 1B and 2). The data in Fig. 2 is collected by the Texas General Land Office (TGLO) Oil Spill

Surface water survey: non-oil measurements

Surface water physicochemical parameters were similar across the sampling area (Table 1) and within expected ranges for this region during the early spring season (Dorado et al., 2015, Rayson et al., 2015). The average temperature 17.2 ± 0.6 °C and salinity 24.0 ± 3.9 were reflective of the spring conditions. The average concentration of NO3, NO2, NH4+ and Pi were 1.16 ± 0.47 μmol L 1, 0.21 ± 0.08 μmol L 1, 10.18 ± 5.30 μmol L 1, and 0.53 ± 0.11 μmol L 1 respectively. Spatially, dissolved nutrient values were

Acknowledgments

This research was supported in part by a grant from The Gulf of Mexico Research Initiative (GoMRI) (#SA15-22)to the Aggregation and Degradation of Dispersants and Oil by Microbial Exopolymers (ADDOMEx) consortium. The original data can be found at the Gulf of Mexico Research Initiative Information and Data Cooperative (GRIIDC) at http://data.gulfresearchinitative.org doi:R4.x263.000:0002. The authors would like to especially thank the Texas General Land Office Oil Spill Prevention and Response

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