Effects of the oxylipin-producing diatom Skeletonema marinoi on gene
expression levels of the calanoid copepod Calanus sinicus
Chiara Lauritano
a,1
, Ylenia Carotenuto
a,1
, Valentina Vitiello
b
, Isabella Buttino
b
, Giovanna Romano
a
,
Jiang-Shiou Hwang
c,d
, Adrianna Ianora
a,
⁎
a
Stazione Zoologica Anton Dohrn, Villa Comunale, 80121 Napoli, Italy
b
Italian Institute for Environmental Protection and Research, Piazzale dei marmi 12, 57123 Livorno, Italy
c
Institute of Marine Biology, National Taiwan Ocean University, 2 Pei-Ning Road, Keelung 20224, Taiwan
d
Department of Biomedical Science and Environmental Biology, Kaohsiung Medical University, Kaohsiung 80708, Taiwan
abstract article info
Article history:
Received 16 December 2014
Received in revised form 28 January 2015
Accepted 28 January 2015
Available online xxxx
Keywords:
Calanus sinicus
Skeletonema marinoi
Stress genes
Gene expression
Copepod–diatom interactions
Diatoms are eukaryotic unicellular plants that constitute one of the major components of marine phytoplankton,
comprising up to 40% of annual productivity at sea and representing 25% of global carbon-fixation. Diatoms have
traditionally been considered a preferential food for zooplankton grazers such as copepods, but, in the last two
decades, this beneficial role has been challenged after the discovery that many species of diatoms produce
toxic metabolites, collectively termed oxylipins, that induce reproductive failure in zooplankton grazers. Diatoms
are the dominant natural diet of Calanus sinicus, a cold-temperate calanoid copepod that supports secondary pro-
duction of important fisheries in the shelf ecosystems of the Northwest Pacific Ocean, Yellow Sea, Sea of Japan
and South China Sea. In this study, the effect of the oxylipin-producing diatom Skeletonema marinoi on
C. sinicus has been evaluated by analyzing expression level changes of genes involved in defense and detoxifica-
tion systems. Results show that C. sinicus is more resistant to a diet of this diatom species in terms of gene expres-
sion patterns, compared to the congeneric species Calanus helgolandicus which is an important constituent of the
temperate waters of the Atlantic Ocean and northern Mediterranean Sea. These findings contribute to the better
understanding of genetic and/or phenotypic flexibility of copepod species and their capabilities to cope with
stress by identifying molecular markers (such as stress and detoxification genes) as biosensors for environmental
perturbations (e.g. toxins and contaminants) affecting marine copepods.
© 2015 The Authors. Published by Elsevier B.V. This is an open access article under the CC BY-NC-ND license
(http://creativecommons.org/licenses/by-nc-nd/4.0/).
1. Introduction
Calanus sinicus is a common cold-temperate calanoid copepod living
in the shelf ecosystem of the Northwest Pacific Ocean, occurring in
the Bohai Sea, the Yellow Sea, the Sea of Japan and the South China
Sea (Hulsemann, 1994), where it supports secondary production of
important fisheries, such as sardine and anchovy (Uye, 2000; Yang
et al., 2014). In coastal waters off northern Taiwan, C. sinicus is a dominant
species from winter to early spring, where it represents more than 50%
of the winter copepod assemblage (Hwang et al., 2006). Its presence in
the area is related to the southward intrusion of cold-water masses of
the China Coastal Current during the northeast monsoon period, from
November to March, which brings cold waters from the Yellow Sea and
the East China Sea into the Taiwan Straits (Dur et al., 2007; Hwang and
Wong, 2005; Tseng et al., 2013). Given its ecological importance, it is
one of the target species in the China-GLOBEC program (Sun, 2005).
Several field studies have indicated that C. sinicus spawns continu-
ously throughout the year in the Northwest Pacific Ocean, with maxi-
mum egg production rates during winter-early spring (Li et al., 2013;
Uye, 2000; Wang et al., 2009; Zhang and Wong, 2013; Zhang et al.,
2005, 2006), thus suggesting that the winter-spring diatom bloom
could enhance copepod reproduction in this area. C. sinicus does in
fact consume large quantities of diatoms as confirmed by a recent
study on the gut contents of specimens collected during the winter sea-
son in northern Taiwan (The most abundant species found in the gut
were Thalassiothrix spp., Chaetoceros spp. and Coscinodiscus spp.; Chen
et al., 2010). The study reported that diatoms represented more than
95% of the ingested food by C. sinicus females, thus confirming previous
results of gut fluorescence analysis, according to which C. sinicus is con-
sidered a clear herbivorous species, although it can switch to omnivo-
rous feeding when microzooplankton prey becomes available (Wang
et al., 2009; Zhang et al., 2006).
It is known that several marine diatoms produce toxic polyunsatu-
rated aldehydes (PUAs) and other products deriving from the oxidation
of fatty acids (collectively termed oxylipins) that reduce reproductive
success and induce larval malformations in several copepod species
Marine Genomics xxx (2015) xxx–xxx
⁎ Corresponding author. Tel.: +39 0815833246.
E-mail address: ianora@szn.it (A. Ianora).
1
First two authors share equal responsibilities.
MARGEN-00286; No of Pages 6
http://dx.doi.org/10.1016/j.margen.2015.01.007
1874-7787/© 2015 The Authors. Published by Elsevier B.V. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
Contents lists available at ScienceDirect
Marine Genomics
journal homepage: www.elsevier.com/locate/margen
Please cite this article as: Lauritano, C., et al., Effects of the oxylipin-producing diatom Skeletonema marinoi on gene expression levels of the
calanoid copepod Calanus sinicus, Mar. Genomics (2015), http://dx.doi.org/10.1016/j.margen.2015.01.007