Potential effects of bacterial communities on the formation of blooms of the harmful dinoflagellate Prorocentrum after the 2014 Texas City “Y” oil spill (USA)
Introduction
Crude oil pollution and harmful algal blooms (HABs) are both growing environmental threats to marine ecosystems (Anderson et al., 2012; Hu et al., 2011). These devastating events may be associated, as HABs have been observed after oil spills in the sea (Özhan et al., 2014b; Almeda et al., 2018; Gemmell et al., 2018). In a recent example, a dense Prorocentrum dinoflagellate bloom occurred after the Texas City “Y” oil spill which occurred on March 22, 2014 as a result of a collision between a barge and another ship in Galveston Bay, Texas, resulting in a release of 168,000 gallons of marine fuel oil (Yin et al., 2015; Gemmell et al., 2018; Williams et al., 2017). However, the association between phytoplankton blooms and oil spills remains controversial due to conflicting results of numerous studies. Some studies demonstrated that oil enhanced phytoplankton growth (Parsons et al., 1976; Linden et al., 1979; Vargo et al., 1982; Özhan et al., 2014a), whereas others found that oil inhibited photosynthesis (Nuzzi, 1973; Miller et al., 1978). In more recent studies auto/mixotrophic dinoflagellates, which are common HAB species, were not only more tolerant of oil than other competing phytoplankton taxa (e.g., diatoms) and grazers (e.g., ciliates), but also their growth was stimulated under oil exposure (≤1200 parts per billion) (Özhan et al., 2014a; Almeda et al., 2018). In addition, some heterotrophic dinoflagellates can ingest crude oil (Almeda et al., 2014). Taken together, oil spills and phytoplankton (particularly dinoflagellates) blooms can be closely associated, but there is a significant knowledge gap regarding the mechanisms that link oil spills and phytoplankton blooms.
Bacteria are a major factor contributing to growth promotion and inhibition of phytoplankton, and there is growing evidence for changes in phytoplankton growth due to modification of associated bacterial communities (BCs) (Buchan et al., 2014 and references therein). Recently, BCs have been recognized to play a role in the formation of HABs in nature (Park et al., 2015; Park et al., 2016, 2017, 2018; Bolch et al., 2017). Although it is well known that oil spills strongly affect both bacterial abundance and community composition in marine environments (Meng et al., 2016; Bacosa et al., 2015, 2016; Gemmell et al., 2018), there is no study on the impact of oil-driven changes in BCs on the formation of blooms. Thus, this study aimed to explore the role of bacteria in the formation of HABs after oil spills. As a first step of this study, the effects of oil-degrading bacteria on the formation of a Prorocentrum bloom after the Texas City “Y” oil spill were examined. Gemmell et al. (2018) suggested that the loss of grazers after this oil spill might have contributed to the formation of the bloom. To better understand the factors causing this bloom, the impact of changes in BCs after crude oil exposure on Prorocentrum growth using laboratory cultures was investigated. In addition, to gain more direct evidence, oil-degrading bacteria were directly isolated from an oil-contaminated site 6 days after the Texas City “Y” oil spill, and their effects on growth of dinoflagellates (including Prorocentrum) growth were investigated.
Section snippets
Algal cultures
The axenic (Amphidinium carterae, UTEX LB 1561; Peridinium sociale, UTEX LB 1948) and xenic (Karenia brevis, SP3TOX; P. gracile, PATX-3; P. minimum, PATX-1; P. texanum, CCMP3349) algal cultures were obtained from the UTEX algal culture collection of the University of Texas at Austin, the National Center for Marine Algae and Microbiota (NCMA) culture collection, the University of Texas Marine Science Institute (the Erdner laboratory and the Villareal laboratory), and Dr. Darren W. Henrichs
Xenic cultures of dinoflagellates
Final growth yield of dinoflagellates was higher after co-culture with the two oil-degrading isolates (C1-T3 and E1-Gal-T2) (Table 1). The maximum dinoflagellate cell densities in bacterial treatments were significantly higher (Student's t-test, p < 0.05), compared to controls for xenic K. brevis (43.8%−50.7% increase), P. gracile (33.1%−49.6%), P. minimum (30.6%−46.3%), and P. texanum (37.9%−38.9%) cultures.
Axenic cultures of dinoflagellates
To better understand the impact of oil-degrading bacterial isolates on dinoflagellate
Discussion
The association between oil spills and the formation of HABs has been observed, but there is lack of explanation on whether or not oil spills are able to lead to the formation of HABs. Recent findings show that BC exposed to crude oil and light clearly enhanced the growth of the harmful dinoflagellate Karenia brevis in laboratory experiments (Park and Buskey, 2020). Thus, we hypothesized that oil exposure changes the bacterial communities (BCs), and in turn these altered bacterial communities
Declaration of Competing Interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgments
We thank Prof. Jian Sheng (Texas A&M at Corpus Christi), Prof. Paul Zimba (Texas A&M at Corpus Christi), Dr. Joo-Hwan Kim (Han River Basin Environmental Office), Dr. Lindsay P. Scheef (University of Texas Marine Science Institute), and Mrs. Cammie J. Hyatt (University of Texas Marine Science Institute) for their assistance with this study. We also thank Dr. Darren W. Henrichs (Texas A&M) and Dr. Tatiana Severin (University of Texas Marine Science Institute) for providing algal cultures. This
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