We explored phagotrophy of the phototrophic ciliate
Mesodinium rubrum
on the cyanobacterium
Synechococcus
. The ingestion and clearance rates of
M. rubrum
on
Synechococcus
as a function of prey concentration were measured. In addition, we calculated grazing coefficients by combining the field data on abundance of
M. rubrum
and co-occurring
Synechococcus
spp. with laboratory data on ingestion rates. The ingestion rate of
M. rubrum
on
Synechococcus
sp. linearly increased with increasing prey concentrations up to approximately 1.9 × 10
6
cells mL
-1
, to exhibit sigmoidal saturation at higher concentrations. The maximum ingestion and clearance rates of
M. rubrum
on
Synechococcus
were 2.1 cells predator
-1
h
-1
and 4.2 nL predator
-1
h
-1
, respectively. The calculated grazing coefficients attributable to
M. rubrum
on cooccurring
Synechococcus
spp. reached 0.04 day
-1
.
M. rubrum
could thus sometimes be an effective protistan grazer of
Synechococcus
in marine planktonic food webs.
M. rubrum
might also be able to form recurrent and massive blooms in diverse marine environments supported by the unique and complex mixotrophic arrays including phagotrphy on hetrotrophic bacteria and
Synechococcus
as well as digestion, kleptoplastidy and karyoklepty after the ingestion of cryptophyte prey.
INTRODUCTION
Mesodinium rubrum
Lohmann 1908 is a cosmopolitan species that recurrently forms ciliate red tides in diverse marine environments (
Taylor et al. 1971
,
Lindholm 1985
,
Crawford 1989
,
Yih et al. 2013
).
M. rubrum
is able to carry out photosynthesis as well as phagotrophic feeding on prey organisms such as cryptophytes (
Yih et al. 2004
,
Johnson and Stoecker 2005
,
Park et al. 2007
,
Hansen et al. 2012
,
2013
) and heterotrophic bacteria (
Myung et al. 2006
). In turn,
M. rubrum
is known to be an important prey item for many protistan and metazoan grazers at higher trophic level (
Sullivan and Gifford 2004
,
Yih et al. 2004
,
Liu et al. 2005
,
Park et al. 2006
,
Reguera et al. 2012
,
Lee et al. 2014
). This species usually co-occurs with bacterioplankton (
Powell et al. 2005
,
Jeong et al. 2013
) and
M. rubrum
blooms sometimes succeed those of bacterioplankton (
Jeong et al. 2013
). Therefore, mixotrophy of
M. rubrum
is most likely a very important phenomenon for the balanced maintenance of healthy marine environments. To understand the ecology of
M. rubrum
in marine food web systems, further exploration on the unique aspects of phagotrophy in
M. rubrum
on several kinds of prey is still desired.
The phototrophic prokaryote
Synechococcus
is a ubiquitous cyanobacterium in marine ecosystem (
Johnson and Sieburth 1979
,
Waterbury et al. 1979
,
Marañón et al. 2003
,
Huang et al. 2012
) with its cosmopolitan distribution from tropical to polar waters (
Walker and Marchant 1989
,
Burkill et al. 1993
,
Landry et al. 1996
,
Powell et al. 2005
).
Synechococcus
spp. numerically dominate the abundance of phytoplankton in marine environments (
Glibert et al. 2004
,
Murrell and Lores 2004
). In addition,
Synechococcus
sometimes contributes significantly to phytoplankton biomass and primary production in marine ecosystem (
Glover et al. 1986
,
Li 1994
,
Jeong et al. 2013
). It is known to be one of the major contributors to CO
2
and nutrient uptake from the ocean waters (
Marañón et al. 2003
). Therefore, the growth and mortality of
Synechococcus
are important factors in understanding the cycling of biomaterials in marine microbial food webs.
Several protistan grazers are known to ingest
Synechococcus
(
Christaki et al. 1999
,
2002
,
Jeong et al. 2005
,
2010
,
2012
,
Apple et al. 2011
,
Strom et al. 2012
). The marine ciliate
M. rubrum
has been found to co-occur with
Synechococcus
spp. in the coastal waters (
Lignell et al. 2003
,
Jeong et al. 2013
,
Liu et al. 2013
). Therefore to better understand
Mesodinium
bacterivory in microbial food webs, we investigated the predator-prey relationships between
M. rubrum
and
Synechococcus
.
We explored whether
M. rubrum
is able to feed on
Synechococcus
. We also measured the ingestion rates of
M. rubrum
on
Synechococcus
as a function of prey concentration. In addition, we estimated grazing coefficients attributable to
M. rubrum
on co-occurring
Synechococcus
using our data for ingestion rates obtained from the laboratory experiments and data on the abundance of
Mesodinium
and
Synechococcus
in the field. The results of the present study provide a basis for improved estimation and understanding the population dynamics of
M. rubrum
in marine ecosystems.
MATERIALS AND METHODS
- Preparation of experimental organisms
For isolation and cultivation of
Mesodinium rubrum
strain MR-MAL01 (
Table 1
) plankton samples were collected from Gomso Bay, Korea, during May 2001 when the water temperature and salinity were 18.0℃ and 31.5, respectively. A culture of
M. rubrum
was established by serial single-cell isolations (
Yih et al. 2004
). The cryptophyte
Teleaulax amphioxeia
strain CR-MAL01 (
Yih et al. 2004
) was offered as prey of
M. rubrum
. Both
M. rubrum
and
T. amphioxeia
were maintained at 20℃ in f/2 medium (
Guillard and Ryther 1962
) without silicate under continuous illumination of 20 μmol photons m
-2
s
-1
of cool white fluorescent light in the walk-in incubator system of the Marine Biology Research and Education Center, Kunsan National University. The phototrophic prokaryote
Synechococcus
strain CC9311 (clade I) (
Table 1
) was also grown at 20℃ in f/2 medium (
Guillard and Ryther 1962)
without silicate under continuous illumination of 20 μmol photons m
-2
s
-1
. This strain has two phycoerythrin proteins (PE I and PE II) (
Ong and Glazer 1991
).
Origin, strain name, and mean cell volume of the two experimental organisms
Cell volume (μm3) of Mesodinium rubrum was measured by an electronic particle counter.
The equivalent spherical diameter and cell volume of
M. rubrum
(
Table 1
) was measured using an electron particle counter (Coulter Multisizer II; Coulter Corporation, Miami, FL, USA). The carbon contents for
M. rubrum
was estimated from cell volume according to
Menden-Deuer and Lessard (2000)
. The cell volume and carbon content for
Synechococcus
sp. was adopted from
Apple et al. (2011)
.
- Prey concentrations (PCs) effects on ingestion and clearance rates
Experiment was designed to measure the ingestion and clearance rates of
M. rubrum
as a function of the PC when fed on
Synechococcus
sp.
We prepared dense cultures of
M. rubrum
(12,000 cells mL
-1
) and
Synechococcus
sp. that were separately grown phototrophically in f/2 medium (
Guillard and Ryther 1962
) without silicate under continuous illumination of 20 μmol photons m
-2
s
-1
. Three 1 mL aliquots were subsampled from each
M. rubrum
culture for the cell counting under a light microscope (Olympus BH2; Olympus Co., Tokyo, Japan). For the
Synechococcus
cell counting, 5 mL aliquots from each
Synechococcus
culture were removed and then fixed with formalin (final conc. = 4%). The fixed sample was stained using DAPI (final conc. = 1 μM) and then filtered onto 25-mm polycarbonate black membrane filters of 0.2 μm-pore-size. The
Synechococcus
cells on the membranes were observed under an epifluorescence microscope (Olympus BH2; Olympus Co.) with UV light excitation at a magnification of ×1,000.
The initial concentrations of
M. rubrum
and
Synechococcus
were established using a pipette to deliver predetermined volumes of known cell concentration to the bottles. Triplicate 80 mL experimental bottles (containing mixtures of
M. rubrum
and
Synechococcus
), triplicate prey control bottles (containing
Synechococcus
only) and triplicate predator control bottles (containing
M. rubrum
only) were also established. All the bottles were placed on a shelf and incubated at 20℃ under illumination of 20 μmol photons m
-2
s
-1
of cool white fluorescent light.
After 1-, 10-, 20-, and 30-min incubation periods, 5 mL aliquots were removed from each bottle, and then fixed with formalin. The fixed samples were stained using DAPI and then filtered onto 3 μm-pore-sized polycarbonate white membrane filters. Then, the cells of
M. rubrum
with
Synechococcus
as well as
Synechococcus
inside a
M. rubrum
were enumerated under an epifluorescence microscope with UV, blue, and green-light excitation at a magnification of ×1,000 by scanning the
M. rubrum
body at consecutive intervals of 1 to 2 μm focal depth along the z-axis. We tried to minimize the concentration of heterotrophic bacteria in the
M. rubrum
culture. For the experiments we subsampled
M. rubrum
from the upper thin layer with high density of
M. rubrum
using a siphon, and then diluted to the target concentrations by adding auto claved seawater to the subsamples. Thus, the initial concentrations of heterotrophic bacteria in the experimental bottles were <16% of
Synechococcus
concentrations.
The ingestion rate (IR; cells predator
-1
h
-1
) was calculated by linear regression of the number of
Synechococcus
per
M. rubrum
cell as a function of incubation time as in
Sherr et al. (1987)
.
The clearance rate (CR; mL predator
-1
h
-1
) was calculated as:
, where IR (cells predator
-1
h
-1
) is the ingestion rate of the
M. rubrum
predator on the
Synechococcus
prey and PC (cells mL
-1
) is the prey concentration.
Ingestion and clearance rates were calculated using the equations of
Frost (1972)
and
Heinbokel (1978)
. Data for IRs (cells predator
-1
h
-1
) were fitted to a Michaelis-Menten equation:
, where I
max
= the maximum ingestion rate (MIR; cells predator
-1
h
-1
), x = PC (cells mL
-1
), and K
IR
= the PC sustaining 1/2 I
max
.
- Potential grazing impact
We estimated the grazing coefficients attributable to
Mesodinium rubrum
on
Synechococcus
spp. by combining field data on the abundance of
M. rubrum
and
Synechococcus
with the ingestion rates of the
M. rubrum
on
Synechococcus
sp. obtained in the present study. Field data on the abundance of
M. rubrum
and co-occurring
Synechococcus
used in this estimation were originally obtained using the water samples from Masan Bay (2004-2005), Korea (
Jeong et al. 2013
).
The grazing coefficient (g day
-1
) was calculated as:
, where CR (mL predator
-1
h
-1
) is the clearance rate of a
M. rubrum
predator on
Synechococcus
prey at a given PC and GC is a predator concentration (cells mL
-1
). CR values were corrected using Q
10
= 2.8 (
Hansen et al. 1997
) because
in situ
water temperatures and the temperature used in the laboratory for this experiment (20℃) were sometimes different.
RESULTS AND DISCUSSION
- PCs effects on ingestion and clearance rates
We found that
M. rubrum
ingested
Synechococcus
cells (
Fig. 1
). This should be the first report of grazing by red tide ciliate
M. rubrum
on
Synechococcus
.
M. rubrum
commonly co-occurred with
Synechococcus
in many marine ecosystems (
Lignell et al. 2003
,
Jeong et al. 2013
,
Liu et al. 2013
). Thus,
M. rubrum
should be considered to be a potentially grazer on
Synechococcus
in marine planktonic food webs.
Epifluorescence images of Mesodinium rubrum with ingested prey Synechococcus sp. (A) An unfed M. rubrum cell under an epifluorescence microscope with green light excitation. (B) M. rubrum with two ingested Synechococcus cells under an epifluorescence microscope with blue light excitation. Arrows indicate ingested prey cells. Scale bars represents: A & B, 10 μm.
The specific ingestion rates (SIRs) of
M. rubrum
on
Synechococcus
linearly increased with increasing PCs up to 1.9 × 10
6
cells mL
-1
, but exhibit sigmoidal saturation at higher concentrations (
Fig. 2
). When the data were fitted to Eq. (2), the MIR of
M. rubrum
was 2.1 cells predator
-1
h
-1
(0.5 pg C predator
-1
h
-1
). In addition,
M. rubrum
was able to acquire up to 12.6 pg C from
Synechococcus
daily. The maximum clearance rate of
M. rubrum
on
Synechococcus
was 4.2 nL predator
-1
h
-1
(
Table 2
).
Specific ingestion rates of the photosynthetic ciliate Mesodinium rubrum on Synechococcus sp. as a function of mean prey concentration (x). Symbols represent treatment means ± 1 standard error. The curves are fitted by a Michaelis-Menten equation [Eq. (2)] using all treatments in the experiment. Ingestion rate (cells predator-1 h-1) = 2.1 [x / (1.2 × 106 + x)], r2 = 0.697.
Comparison of maximum ingestion rates and carbon acquisition inMesodinium rubrumwith three different prey species
PV, prey volume (μm3); MIR, maximum ingestion rate (pg C predator-1 h-1); KIR, the prey concentration sustaining 1/2 MIR (cell mL-1); MCR, maximum clearance rate (nL predator-1 h-1); CA, carbon acquired from prey by predator per day (pg C predator-1 d-1); BC, acquired carbon as percentage of predator’s carbon (%). aThe maximum value among the mean ingestion rates measured at given prey concentrations.
In comparison with MIRs of other red tide organisms when fed on
Synechococcus
, the MIR of
M. rubrum
on
Synechococcus
is quite much lower (
Table 3
). The maximum of volume SIR (VSIR) of
M. rubrum
was also lower than that of the other predators.
M. rubrum
is also able to feed on heterotrophic bacteria with higher SIR than that for
Synechococcus
(
Myung et al. 2006
). In addition,
M. rubrum
fed on exclusively cryptophyte prey species when offered a variety of algal prey species (
Park et al. 2007
,
Myung et al. 2013
). Thus, such kind of multiple prey species for the phagotrophy of
M. rubrum
might have evoked a type of partitioned ingestion with differential prey preferences.
Comparison of ingestion rates and carbon acquisition of red tide organisms onSynechococcususing prey-inclusion method in the literature
PD, predator volume (μm3); MIR, maximum ingestion rate (pg C predator-1 h-1); KIR, mean prey concentration sustaining 1/2 MIR (×105 cells mL-1); MCR, maximum clearance rate (nL predator-1 h-1); VSIR, volume specific ingestion rate (×10-3 h-1); CIL, ciliate; RAP, raphidophyte; DIN, dinophyte. aThe maximum value among the mean ingestion rates measured at given prey concentrations.
The ingestion rates of the red tide organisms on
Synechococcus
were affected by the PC. The K
IR
(the mean PC sustaining 1/2 I
max
of MIR) of 1.2 × 10
6
cells mL
-1
for
M. rubrum
feeding on
Synechococcus
was relatively higher than that for other predators (
Table 3
). Therefore, the ingestion of
M. rubrum
on
Synechococcus
was less sensitive than that of other red tide organisms to the concentration of prey cells under prey-limited conditions.
The MIRs of heterotrophic nanoflagellates, mixotrophic dinoflagellates, heterotrophic dinoflagellates, and ciliates feeding on
Synechococcus
sp. are in general positively correlated with the predator’s equivalent spherical diameter (p < 0.01, ANOVA) (
Table 4
,
Fig. 3
). This relationship suggests that the sizes of the protistan grazers may be an important factor affecting their ingestion rates on
Synechococcus
. However, the MIR of
M. rubrum
on
Synechococcus
is relatively quite lower than that of the other protistan grazers with the exceptions in
Picophagus flagellates
,
Bodo saltans
, and
Gonimonas pacifica
. Furthermore,
M. rubrum
exhibited jumping behavior (
Fenchel and Hansen 2006
). This jumping behavior of
M. rubrum
may be partially responsible for the minimal ingestion. The MIR of
Ochromonas
sp. feeding on
Synechococcus
was higher than that of the other protistan grazers with the exception
Eutinnuis
sp. (
Table 4
). In addition, the SIR of
Ochromonas
was higher than that of the other protistan grazers. Thus,
Synechococcus
was the optimal prey for
Ochromonas
sp. not for
M. rubrum
among bacteriovorus protistan grazers.
Comparison of ingestion rates and carbon acquisition of protistan grazers onSynechococcusin the literature
ESD, equivalent spherical diameter (μm); MIR, maximum ingestion rate (pg C predator-1 h-1); MCR, maximum clearance rate (nL predator-1 h-1); CIL, ciliate; HNF, heterotrophic nanoflagellate; CRY, cryptophyte; RAP, raphidophyte; MTD, mixotrophic dinoflagellate; HTD, heterotrophic dinoflagellate. aThe maximum value among the mean ingestion rates measured at given prey concentrations.
Ingestion rates of protistan grazers on Synechococcus as a function of predator size (equivalent spherical diameter, ESD, μm). The equation of the regression was follows: Ingestion rate (ng C predator-1 h-1) = 1.33e(0.046 x ESD), r2 = 0.790. Ac, Alexandrium catenella; Am, A. minutum; As, Akashiwo sanguinea; At, A. tamarense; Bs, Bodo saltans; Co, Chattonella ovata; Cp, Cochlodinium polykrikoides; Cr, Cafeteria roenbergensis; Esp, Eutintinnus sp.; Gc, Gymnodinium catenatum; Gi, G. impudicum; Gp, Goniomonas pacifica; Gpo, Gonyaulax polygramma; Gs, G. spinifera; Ha, Heterosigma akashiwo; Hr, Heterocapsa rotundata; Ht, H. triquetra; Kb, Karenia brevis; Lp, Lingulodinium polyedrum; Mr, Mesodinium rubrum; Om, Oxyrrhis marina; Osp, Ochromonas sp.; Pd, Prorocentrum donghaiense; Pf, Picophagus flagellates; Pmc, P. micans; Pmn, P. minimum; Psp, Pseudobodo sp.; Ss, Strombidium sulcatum; Ssp, Spumella sp.; St: Scrippsiella trochoidea; Sv, Symbiodinium voratum; Usp, Uronema sp.
The MIR of
M. rubrum
on
Synechococcus
provided in the present study was higher than that of the small heterotrophic nanoflagellate
Picophagus flagellates
(0.18 pg C predator
-1
h
-1
),
Bodo saltans
(0.12 pg C predator
-1
h
-1
) on
Synechococcus
(
Guillou et al. 2001
). However, the MIR of
M. rubrum
on
Synechococcus
was lower than that of
Pseudobodo
sp. (0.68 cells predator
-1
h
-1
) (
Dolan and Šimek 1998
,
Christaki et al. 2002
). Therefore,
M. rubrum
may sometimes compete with the heterotrophic nanoflagellates for the common prey
Synechococcus
if they co-occur.
- Impact ofMesodinium rubumon prey species
M. rubrum
was found to be able to feed on the cyanobacterium
Synechococcus
sp. as well as the cryptophyte
Teleaulax amphioxeia
and heterotrophic bacteria (
Yih et al. 2004
,
Myung et al. 2006
).
M. rubrum
grew well when supplied with
T. amphioxeia
(
Yih et al. 2004
). However,
M. rubrum
did not sustain growth when only heterotrophic bacteria or
Synechococcus
were offered as prey (personal observation, data not shown here). Therefore,
Synechococcus
may not make a critical contribution to the population growth of
M. rubrum
in natural environments, but become supplementary prey.
M. rubrum
is known to require both food uptake and photosynthesis for sustainable growth. The prey cells are used as sources for energy, carbon, and nutrients. Accordingly,
M. rubrum
seems to be able to perform photosynthesis using kleptoplastids from a cryptomonad
T. amphioxeia
while taking up heterotrophic bacteria and
Synechococcus
as phosphorus and nitrogen source.
- Grazing impact onSynechococcuspopulations
The grazing coefficients attributable to
M. rubrum
on co-occurring
Synechococcus
spp. in Masan Bay, Korea were affected mostly by the abundance of
M. rubrum
predator. The abundance of
M. rubrum
and
Synechococcus
spp. (n = 40) were 11-933 cells mL
-1
and 51-39,509 cells mL
-1
, respectively. Grazing coefficients attributable to
M. rubrum
on co-occurring
Synechococcus
spp. were 0.001 to 0.036 day
-1
(
Fig. 4
).
Calculated grazing coeffienents of Mesodinium rubrum (n = 40) in relation to the concentration of co-occurring Synechococcus (see text for calculation). Clearance rates measured under the conditions provided in the present study, were corrected using Q10 = 2.8 (Hansen et al. 1997) because in situ water temperatures and the temperature used in the laboratory for this experiment (20℃) were sometimes different. The scales of the circles in the inset boxes are g day-1.
To our knowledge, prior to this study, there had been no reports on the estimation of grazing impact by
Mesodinium
on co-occurring populations of
Synechococcus
. Grazing coefficients derived from studies in Masan Bay in 2004-2005 show that up to 3.6% of
Synechococcus
populations can be removed by
Mesodinium
in approximately 1 day. High mean abundance of
Synechococcus
(3,568 cell mL
-1
) and relatively low mean abundance of
Mesodinium
(99 cell mL
-1
) in coastal waters are responsible for the resulted relatively lower grazing coefficients. The results of the present study suggested that
M. rubrum
was not able to control the whole
Synechococcus
populations. However, the ingestion rates of protists are known to be affect by light and nutrition conditions (
Jeong et al. 1999
,
Myung et al. 2006
,
Berge et al. 2008
). Therefore, the lower grazing impact of
Mesodinium
on co-occurring
Synechococcus
may also be affected by light and nutrients conditions as well as the prey availability.
- Ecological significance ofSynechococcusfeeding byMesodinium rubrum
Complex mixotrophy in the marine ciliate Mesodinium rubrum.
Unique status of kleptoplastidy in
M. rubrum
was shown by the highly organized chloroplast-mitochondria complexes from its cryptophyte prey (
Johnson et al. 2007
,
Nam et al. 2012
), long-time functioning of the kleptoplastids (
Myung et al. 2013
), and even the karyoklepty from the ingested cryptophyte prey cells (
Johnson et al. 2007
). Bacterivory in
M. rubrum
was noteworthy as an alternate source of essential microelements and cell carbon (
Myung et al. 2006
). Present study confirms that
M. rubrum
also feed on
Synechococcus
cells, one of the most abundant single cell phototrophs in the sea. In the euphotic zone of the oligotrophic open ocean
Synechococcus
spp. predominates the upper euphotic layers, and sometimes perform nitrogen fixation, to be fed into open ocean food web (
Phlips et al. 1989
,
Walker and Marchant 1989
). Equipped with quite unique and complex mixotrophic arrays of metabolism such as phagotrphy on hetrotrophic bacteria and
Synechococcus
as well as digestion, kleptoplastidy, and karyoklepty after the ingestion of cryptophyte prey,
M. rubrum
might be able to form recurrent and massive blooms in diverse marine environments (
Crawford 1989
,
Herfort et al. 2011
,
Yih et al. 2013
).
Metabolic importance of Synechococcus for Mesodinium rubrum.
C requirements for the growth of
M. rubrum
can be met by photosynthesis using kleptoplastids from prey cryptophytes as well as C from ingested cryptophytes, heterotrophic bacteria, and autotrophic bacteria like
Synechococcus
spp. (
Yih et al. 2004
,
Myung et al. 2006
,
2011
,
2013
,
Park et al. 2007
). Maximum contribution to the growth of
M. rubrum
by ingested cryptophytes, heterotrophic and phototrophic bacteria were estimated to reach 5.5, 6.2, and 1.2% body carbon ciliate
-1
day
-1
, respectively (
Yih et al. 2004
,
Myung et al. 2006
).
New trophic pathways from marine phototrophic prokaryotes.
Present study showed that
M. rubrum
is able to feed on phototrophic prokaryotes the most abundant microorganisms in the ocean (
Johnson and Sieburth 1979
,
Waterbury et al. 1979
,
Ferris and Palenik 1998
).
M. rubrum
has thus long been involved in the newly recognized trophic pathways between diverse marine organisms and
Synechococcus
, which further emphasizes the ecological importance of
M. rubrum
as a new model organism with multiple layers of mixotrophy. Currently, more information about the population dynamics of
M. rubrum
is needed to understand the relative importance of its
Synechococcus
feeding for the frequent success of the mixotrophic ciliate in the sea.
CONCLUSION
Phagotrophy of the phototrophic ciliate
Mesodinium rubrum
on the cyanobacterium
Synechococcus
, one of the most abundant single cell phototrophs in the sea, was firstly confirmed by the feeding experiment in the present study. By the unique and complex mixotrophic arrays including phagotrophy on heterotrophic bacteria and
Synechococcus
as well as digestion, kleptoplastidy and karyoklepty after the ingestion of cryptophyte prey, thus,
M. rubrum
can form recurrent and massive blooms in diverse marine environments. The new trophic pathway from
Synechococcus
to diverse predators linked by
M. rubrum
might further emphasize the ecological importance of
M. rubrum
as a marine model organism with multiple layers of mixotrophy.
Acknowledgements
This paper was supported by the National Research Foundation of Korea (NRF) grants funded by the Korea government (MSIP), (NRF-2015M1A5A1041808, award to W. Yih) and (NRF-2014R1A6A3A01059254, award to Y. D. Yoo), and a KIMST (Korea Institute of Marine Science and Technology Promotion Program, Technical Development for Aquacultural Industrialization award to H. S. Kim and the National Marine Biodiversity Institute Research Program (2015M00100) award to K. A. Seong.
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