ORIGINAL ARTICLE
Dynamics of Heterocapsa sp. and the associated attached
and free-living bacteria under the influence of dispersed
and undispersed crude oil
T. Severin, H.P. Bacosa, A. Sato and D.L. Erdner
Marine Science Institute, The University of Texas at Austin, Port Aransas, TX, USA
Significance and Impact of the Study: In the environment, oil spills have the capacity to modify phyto-
plankton communities, with important consequences on the food web and the carbon cycle. We are
just beginning to understand the oil resistance of phytoplankton species, making it difficult to predict
community response. In this study we highlighted the strong resistance of Heterocapsa sp. to oil, which
could be associated with its resilient attached bacteria and oil degradation by the free-living bacteria.
This finding suggests new directions to explore in the understanding of oil impacts and interactions
between eukaryotic and prokaryotic microbes.
Keywords
attached bacteria, dinoflagellate, dispersant,
free-living bacteria, oil, phytoplankton-
bacteria interaction.
Correspondence
Tatiana Severin, Marine Science Institute, The
University of Texas at Austin, 750 Channel
View Drive, Port Aransas, TX 78373-5015,
USA.
E-mail: tatiana.severin@utexas.austin.edu
2016/0827: received 18 April 2016, revised
11 July 2016 and accepted 20 August 2016
doi:10.1111/lam.12661
Abstract
While many studies have examined the impact of oil on phytoplankton or
bacteria, very few considered the effects on the biological complex formed by
phytoplankton and their associated phytoplankton-attached (PA) and free-
living (FL) bacteria. However, associated bacteria can affect the physiology of
phytoplankton and influence their stress responses. In this study, we
monitored the growth of Heterocapsa sp., an armoured dinoflagellate, exposed
to crude oil, Corexit dispersant, or both. Growth of Heterocapsa sp. is
unaffected by crude oil up to 25 ppm, a concentration similar to the lower
range measured on Florida beaches after the Deepwater Horizon oil spill. The
PA bacteria community was resistant to exposure, whereas the FL community
shifted towards oil degraders; both responses could contribute to Heterocapsa
sp. oil resistance. The growth rate of Heterocapsa sp. decreased significantly
only when exposed to dispersed oil at 25 ppm, indicating a synergistic effect of
dispersant on oil toxicity in this organism. For the first time, we demonstrated
the decoupling of the responses of the PA and FL bacteria communities after
exposure to an environmental stress, in this case oil and dispersant. Our
findings suggest new directions to explore in the understanding of interactions
between unicellular eukaryotes and prokaryotes.
Introduction
Because they are responsible for about 50% of annual glo-
bal carbon dioxide fixation (Field 1998), marine phyto-
plankton are a crucial part of the global carbon cycle and
form the base of the food web in aquatic systems. These
important functions can be altered by both acute and
chronic disturbances such as oil spills. The Deepwater
Horizon (DWH) oil spill in April 2010 is the largest acci-
dental oil spill in the United States history and affected
the Gulf of Mexico coast from Louisiana to Florida (Sam-
marco et al. 2013). A remote sensing study suggests that
this massive oil spill stimulated an intense phytoplankton
bloom observed 4 months afterwards in the north-eastern
Gulf of Mexico (Hu et al. 2011). However, most labora-
tory experiments observe a decrease in total chlorophyll a
after oil addition (Gonz alez et al. 2009; Jung et al. 2012).
They also show that oil responses are species-dependent
with a greater tolerance in diatoms and dinoflagellates
(Gilde and Pinckney 2012;
€
Ozhan et al. 2014).
Letters in Applied Microbiology 63, 419--425 © 2016 The Society for Applied Microbiology 419
Letters in Applied Microbiology ISSN 0266-8254