Marine hydrothermal vents as templates for global change scenarios

Abstract

Subsurface marine hydrothermal vents (HVs) may provide a particular advantage to better understand evolutionary conditions of the early earth and future climate predictions for marine life. Hydrothermal vents (HV) are unique extreme environments that share several similarities with projected global and climate change scenarios in marine systems (e.g., low pH due to high carbon dioxide and sulfite compounds, high temperature and turbidity, high loads of toxic chemicals such as H2S and trace metals). Particularly, shallow hydrothermal vents are easily accessible for short-term and long-term experiments. Research on organisms from shallow HVs may provide insights in the molecular, ecological, and evolutionary adaptations to extreme oceanic environments by comparing them with evolutionary related but less adapted biota. A shallow-water hydrothermal vent system at the northeast Taiwan coast has been intensively studied by several international research teams. These studies revealed astounding highlights at the levels of ecosystem (being fueled by photosynthesis and chemosynthesis), community (striking biodiversity changes due to mass mortality), population (retarded growth characteristics), individual (habitat attractive behavior), and molecular (adaptations to elevated concentrations of heavy metals, low pH, and elevated temperature). The present opinion paper evaluates the potential of shallow hydrothermal vents to be used as a templates for global change scenarios.

Full text

OPINION PAPER
Marine hydrothermal vents as templates for global change
scenarios
Hans-Uwe Dahms .Nikolaos V. Schizas .R. Arthur James .Lan Wang .
Jiang-Shiou Hwang
Received: 30 December 2016 / Revised: 20 March 2018 / Accepted: 21 March 2018
ÓSpringer International Publishing AG, part of Springer Nature 2018
Abstract Subsurface marine hydrothermal vents
(HVs) may provide a particular advantage to better
understand evolutionary conditions of the early earth
and future climate predictions for marine life.
Hydrothermal vents (HV) are unique extreme envi-
ronments that share several similarities with projected
global and climate change scenarios in marine systems
(e.g., low pH due to high carbon dioxide and sulfite
compounds, high temperature and turbidity, high loads
of toxic chemicals such as H
2
S and trace metals).
Particularly, shallow hydrothermal vents are easily
accessible for short-term and long-term experiments.
Research on organisms from shallow HVs may
provide insights in the molecular, ecological, and
evolutionary adaptations to extreme oceanic environ-
ments by comparing them with evolutionary related
but less adapted biota. A shallow-water hydrothermal
vent system at the northeast Taiwan coast has been
intensively studied by several international research
teams. These studies revealed astounding highlights at
the levels of ecosystem (being fueled by photosynthe-
sis and chemosynthesis), community (striking biodi-
versity changes due to mass mortality), population
(retarded growth characteristics), individual (habitat
attractive behavior), and molecular (adaptations to
elevated concentrations of heavy metals, low pH, and
elevated temperature). The present opinion paper
evaluates the potential of shallow hydrothermal vents
to be used as a templates for global change scenarios.
Keywords Shallow hydrothermal vent Early earth
environment Global change template Adaptations 
Extreme habitat
Handling editor: Boping Han
H.-U. Dahms
Department of Biomedical Science and Environmental
Biology, Kaohsiung Medical University, Kaohsiung,
Taiwan
H.-U. Dahms
Research Center for Environmental Medicine, Kaohsiung
Medical University, Kaohsiung, Taiwan
N. V. Schizas
Department of Marine Sciences, University of Puerto
Rico PR, Mayagu
¨ez, USA
R. A. James
Department of Marine Science, Bharathidasan University,
Tamil Nadu, India
L. Wang J.-S. Hwang
School of Life Science, Shanxi University, Shanxi, China
J.-S. Hwang (&)
Institute of Marine Biology, National Taiwan Ocean
University, Keelung, Taiwan
e-mail: jshwang@mail.ntou.edu.tw
123
Hydrobiologia
https://doi.org/10.1007/s10750-018-3598-8

Introduction
Global change summarizes recent phenomena that
cause planetary-scale changes in the earth system. The
earth system consists of the oceans, land, atmosphere,
poles, the planet’s natural cycles, deep earth processes,
biosphere, and includes the human society. In the last
250 years, global change has caused climate change,
loss of critical habitats, desertification, ocean acidifi-
cation, ozone depletion, pollution, widespread distri-
bution changes and extinction of species, fish-stock
collapses, and other large-scale biotic shifts (Mora
et al., 2017). Global climate change is a shift in the
occurrence of weather patterns over periods ranging
from decades to longer time intervals. Besides, climate
forcing factors such as variations in solar radiation,
plate tectonics, volcanic eruptions, and biotic pro-
cesses, human activities have been linked to recent
climate change scenarios (Doney et al., 2009). In
marine systems, hydrothermal vents are proposed to
be used as templates to study global climate change in
the present paper. This proposal is based on research
during the past two-decades on shallow hydrothermal
vents of Taiwan (Hwang & Lee, 2003; Dahms &
Hwang, 2013; Chan et al., 2014; Dahms et al.,
2013,2014a,b,2017). As such, hydrothermal vents
(HVs) share several factors with global change
phenomena (e.g., high temperature and CO
2
, low pH
and oxygen, toxic chemicals such as sulfite com-
pounds, high trace metal loads, turbidity—see Fig. 1).
Increasing levels of CO
2
and other gases are respon-
sible for ocean acidification with a reduction of ocean
water pH (Tunnicliffe et al., 2009). Research on
organisms from HVs could provide insights in the
behavioral, genomic, and evolutionary adaptations to
an extreme environment (Campbell et al., 2009,
Dahms et al., 2017) that could be compared with
biota living outside the vents (Dando, 2010). Partic-
ularly, shallow HVs may provide a suitable natural
laboratory for observations and experimental
approaches to biotic effects and adaptations to envi-
ronmental extremes and global change issues (Boatta
et al., 2013). As natural habitats, HVs can be used to
understand and predict global change scenarios of a
future ocean and organisms living there (Ka
´da
´r et al.,
2007; Dahms & Hwang, 2013).
HVs are fissures in the planet’s surface from which
geothermally heated water provides a unique habitat of
specialized, highly endemic benthic communities.
Hydrothermal vents are distributed at depths ranging
from a few meters to more than 5000 m throughout the
world’s oceans (Tarasov et al., 2005). The emitted
fluids typically contain a large amount of sulfur
compounds and metals that are leaching from the
mineral base (Van Dover, 2000). The surrounding
water chemistry is strongly influenced by these phys-
ical and chemical conditions, leading to a toxic
acidified environment which is lethal to most biota
from outside the HVs (Dahms & Hwang, 2013; Van
Dover, 2014). Biological communities associated with
shallow and deep HVs have developed behavioral,
morphological, and reproductive adaptations as well as
symbiotic (Adams et al., 2011; Dahms & Hwang,
2013; Dahms et al., 2013,2014a,b,2017), physiolog-
ical and biochemical systems for sulfide detoxification
(Boutet et al., 2009; Li et al., 2017), molecular
responses to high temperature (Smith et al., 2013;
Kim et al., 2017), and specialized sensory organs to
locate hot chimneys (Gebruk et al., 2000).
Shallow-water vent research has a longer history
than deep-sea vent research, dating back to the 19th
century (Tarasov et al., 2005). Environmental inves-
tigations on shallow-water hydrothermal vents have
been conducted in many regions, including, Greece,
Italy, the Kurile Islands, Baja California, Japan,
Taiwan, and Papua New Guinea (Hwang & Lee,
2003, Tarasov et al., 2005). Data suggest that shallow
and deep-sea vents exhibit major differences in their
physical and chemical properties, resulting in dissim-
ilar biological characteristics (Figs. 2,3, Table 1).
Shallow-water hydrothermal vents in particular con-
tain substantially fewer biota which have an obligatory
relationship with the vents than deep-water HVs
(Hwang & Lee, 2003). Since shallow-water vents
occur in the euphotic zone, the contribution of
photosynthesis to primary production is important,
whereas at deep-sea vents, organic matter is generated
by chemosynthesis (Dando, 2010).
Hydrothermal vents are considered to be similar to
a chemosynthetic ecosystem of an early planet. They
thus provide a conceptual framework for the evolution
of early life forms (Nisbet & Sleep, 2001). Adaptive
processes to such a unique physical and chemical
environment can further enhance our understanding of
global change scenarios since the factors under
discussion are comparable (e.g., temperature, pH,
toxicity). We emphasize here that a gradient in hot or
diffuse vent fluids that gets diluted with seawater
Hydrobiologia
123

would be more representative of a global change
scenario, rather than the extreme conditions found
closer to the vents.
We opt to use particularly shallow-water hydrother-
mal vents as proxies for a natural laboratory that would
allow the study of marine organism’ adaptations to
highly adverse physicochemical conditions. The two
major objectives of the present evaluation are (1) to
compare similarities of adverse biological effects of
both climate forcing and of shallow HVs, and (2) to
assess the possibilities particularly of shallow HVs as
templates for research on effects and adaptations of
organisms to global change.
Effects of vent fluid temperature and chemistry
The sea bottom surrounding HVs represents a hetero-
geneous environment. Within this area, vent fluids and
ocean waters are mixing. These two fluids have very
different physical and chemical properties with steep
gradients. Characteristics of the water experienced by
organisms that live near the vents can change at small
spatial and temporal scales. Emitted vent fluids can
reach temperatures of about 116°C in shallow vents
like at Kueishantao; the cooling effects of the
surrounding seawater create strong thermal gradients
(Girguis & Lee, 2006). The fluid emission is often
unstable and sudden bursts of hot vent fluids are
commonly providing vents with large thermal vari-
ability (Hwang & Lee, 2003). Vent organisms are thus
subject to rapid and acute temperature changes, with
temperatures fluctuating at temporal scales of seconds
to minutes. Tolerance to these unstable conditions is
important for vent biota (Amend et al., 2011). This
might provide a limitation to our approach using HVs
as templates for more gradual change during global
warming which happens right now and will further
increase in the coming century.
The ability of an organism to make physiological
adjustments in response to temperature is important
for defining an organism’s thermal niche (Boutet et al.,
2009). Low metabolic rate and little variation in
metabolic rate may be a common adaptation within
hydrothermal vents (Smith et al., 2013). The body
temperature of aquatic ectotherms fluctuates over the
full range of temperature in their habitat. Thus, a
regulation of metabolism in response to thermal
challenges is vital for these organisms (Dahms et al.,
2011). Species with a high metabolic sensitivity over
their environmental range have increased the long-
term metabolic costs and a lower tolerance to extreme
temperatures (Boutet et al., 2009; Dahms et al., 2016).
Since HV fluids have a higher water temperature
and become buoyant, fluids discharged from the vents
are transported upwards and are floating on the
surface. The fluids discharged from the vents have a
GlOBAL CHANGE
SCENARIO
SHALLOW HVs
ALLOW
OBSERVATION
EXPERIMENT
MODELLING
Characteriscs Characteriscs
Temperature Global warming
pH Acidificaon
Trace elements Increased mobilisaon
Trace element leaching
Disturbance of Ca-homeostasis
Co
2,
So
x
, No
X
Combuson gases
Turbidity Landuse, mining, coastal
construcon
Fig. 1 Comparison of characteristics of Kueishan Island (KST), shallow hydrothermal vents with characteristics of global change
biology (compiled from different literature sources)
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significant impact on water chemistry and hence on the
biology of organisms in the ambient environment. The
surface water then appears whitish due to sulfur, sulfur
bacteria, and gas bubbles, whereas the bottom layer
remains transparent in many cases. Accordingly, an
influence of the vent fluid on water chemistry is more
pronounced in the surface layer than in the bottom
layer, resulting in vertical differences in physical and
chemical properties. The effects of surface water
chemistry of the vent region are more similar to the
fluids from the smokers than to water of the bottom
layer. Accordingly, a stronger negative impact on
species in surface waters can be expected than in the
bottom layer. This is consistent with observations that
plankton in the surface water can be killed by vent
plumes and produces ‘‘marine snow’’ composed of
sedimenting dead plankton (Jeng et al., 2004; Dahms
& Hwang, 2013). Experimental cages at different
depths in the HVs of Kueishan Island also indicated
that copepods at the top layer had the greatest
mortality (Dahms & Hwang, 2013).
Hydrological factors measured at shallow HVs
reflect the environmental conditions at only one
particular point in time. A previous study reported
that high temporal variations in water temperature off
Kueishan Island are attributable to diurnal tides (Chen
et al., 2005b). It is, therefore, reasonable to expect a
similar level of variation in other parameters within
shallow HVs. The complex surface circulation may
transport different amounts of vent effluents to partic-
ular sites in the same locality, resulting in variable
patterns that are observed among the sites.
Fig. 2 Shallow hydrothermal vents at KST, off the NE coast of
Taiwan are useful ‘‘natural laboratories’’ for the study of global
change characteristics. (A) Location of KST at northeastern
Taiwan; (B) depth contoures around KST; (C) Skyview
(compiled from different literature sources)
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Low pH as a proxy for ocean acidification
Rising atmospheric CO
2
and other gases are respon-
sible for ongoing ocean acidification resulting in the
reduction of ocean water pH and changes in the
carbonate chemistry (Tunnicliffe et al., 2009). CO
2
production is primarily driven by human fossil fuel
combustion and deforestation, followed by the emis-
sion of aerosols to the atmosphere. There is great
concern about related biological and ecological effects,
as elevated CO
2
partial pressure in seawater has direct
impacts on marine calcifying organisms (Hall-Spencer
et al., 2008; Fabry et al., 2008) and calcium carbonate-
based systems (Silverman et al., 2009), biodiversity,
trophic interactions, and other ecosystem processes
(Glover et al., 2010; Chan et al., 2012).
It was shown at shallow CO
2
vents that calcification
is highly impacted by reductions in seawater pH and
associated changes in carbonate chemistry (Boatta
et al., 2013). Shallow HVs can be taken as natural
Fig. 3 KST shallow hydrothermal vents provide gas emissions above the sea surface (A) and from the sea bottom (B,C)
Table 1 Comparison of
major physical, chemical,
geological, and biological
parameters at shallow-water
and deep-water
hydrothermal vents
(compiled from different
literature sources)
Parameter Shallow-water HVs Deep-water HVs
Light Yes No
Temperature
HV fluid Low High
Ambient High Low
Hydrostatic pressure Low High
Hydrodynamic disturbance High Low
pH Variable Variable
Habitat stability Low Low
Species richness Low High
Endemicity Low High
Biomass Low High
Productivity Variable High
Photo- and chemoautotrophic Chemoautotrophic
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laboratories for climate change. In addition, these
could explain how organisms are avoiding to be
poisoned by high sulfide and heavy metal
concentrations.
Sediments in fluid venting areas are generally
characterized by conspicuous metal deposits of
hydrothermal origin (Aldhous, 2011). This is a
consequence of acid leaching from the underlying
rocks, which leads to the discharge of metal-rich
hydrothermal fluids (Edmond et al., 1979). Due to
constant percolation of CO
2
through the sediments, a
cascade of biogeochemical changes in sediments close
to the vents and at the sediment–water interface can
occur, affecting the precipitation of trace elements
with likely harmful effects on the biota (Nuzzio et al.,
2012). A substantial decrease in seawater pH and Eh
observed close to submarine CO
2
vent sites may
influence the solubility and bioavailability (dissolu-
tion and/or desorption) of some metals and metalloids.
This probably contributes to keeping Fe and other
elements (Mn, Co, Cd, Cu, Cr, and V) in dissolved
form, leading to low enrichment in sediments. For
example, the geochemistry of Fe plays a prominent
role in the transfer of trace elements at the water–
sediment interface (Hsiao & Fang, 2013). A decrease
from pH 8.1–7.4 is responsible for a 40% elevation of
Fe solubility in the water column. In addition, the
redox potential provides another decisive factor in Fe
chemistry. Aiuppa et al. (2000) showed that reducing
environments are contributing to increasing Fe solu-
bility. In contrast, the simultaneous rise in pH and Eh
can cause the precipitation of dissolved Fe into solid
compounds with increasing distance from a vent site.
In addition to the synergistic effects of declining pH
and perturbation of carbonate chemistry, ocean acid-
ification may have an indirect effect by increasing the
availability of contaminants (Vizzini et al., 2013).
HV systems commonly also show a very high
turbidity and heavy metal content, similar to many
coastlines where coral reefs or intertidal zones are
threatened by turbidity and due to factors like road
construction, flushing, typhoon, heavy rain, etc.
Therefore, effects on organisms affected by HV
turbidity and heavy metal content are expected to
have similar outcomes for the environmental condi-
tions of a future ocean.
The effects of multiple stressors: warmer
temperature and lower pH
As ocean waters are becoming warmer and more
acidic at the same time, both environmental stressors
cannot be studied in isolation. Organisms face warmer
and more acidic waters and the interaction of these
physical variables may be different with species and
developmental stages (Wood et al., 2010). To provide
two examples here, Arnold et al. (2013) showed the
interactive effects of ocean acidification and global
warming on the growth and dimethylsulfate synthesis
of the coccolipthore microalgae Emiliania huxley.
Ericson et al. (2012) demonstrated the interactive
effects of these two stressors which reduce fertiliza-
tion rate and the growth of early developmental stages
of the sea urchin Sterechinus neumayeri from the
Antarctic.
Shallow HVs off Kueishantao as natural
laboratories: a case study
Shallow HVs are ideal habitats to study the interactive
effects of these two variables in marine organisms
since the surrounding waters and sediments are
naturally warmer and more acidic (Hwang & Lee,
2003; Ka & Hwang, 2011). Gradients of pH and
temperature may be stable or fluctuating depending on
the geophysical stability of the HVs (Hall-Spencer
et al., 2008). The capacity and the associated energetic
costs of HV biota to withstand fluctuations of pH and
temperature can be compared with phylogenetically
related non-HV biota. Since HVs share several
characteristics with global change phenomena, they
may provide suitable templates for experimental
approaches to biotic effects and adaptations to envi-
ronmental extremes and global change factors (Hwang
& Lee, 2003; Zielinski et al., 2011). Particularly,
in situ studies and the retrieval of organisms would be
much facilitated when studying HVs in shallow
waters. This was done before not only at several
shallow-water HV sites worldwide (see Morri et al.,
1999; Tarasov et al., 1999; Karlen et al., 2010; Bianchi
et al., 2012) but also at the NE coast of Taiwan (Hwang
& Lee, 2003; Hwang et al., 2007).
Shallow HVs off Kueishantao, an island close to the
northeastern Taiwan coast, 60 miles from HVs of the
Okinawa Trough (Zeng et al., 2013) are located at a
tectonic junction of the fault system extension of
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Taiwan and the southern rifting end of the Okinawa
Trough (Wang et al., 2000). The Kueishantao
hydrothermal vent field (121°550E, 24°500N, about
0.5 km
2
) is situated in shallow waters southeast of
Kueishantao (Zeng et al., 2013). The area surrounding
the field is characterized by a seafloor with lava and
pyroclastic sediments. The last major eruption
occurred about 7000 years ago (Zeng et al., 2007)
off northeastern Taiwan, near the southern Okinawa
Trough. There are several hydrothermal vents in
shallower waters (15–300 m depth) with the lowest
recorded vent water pH worldwide (Chen et al.,
2005a). Gases produced here at the vent sites are
mainly composed of carbon dioxide and a small
amount of hydrogen sulfide (Tang et al., 2013). The
vents can be divided into ‘‘yellow spring’’ and ‘‘white
spring’’ types. The temperature of the yellow-spring
fluids is between 78 and 116°C, and the temperature of
the white-spring fluids is between 30 and 65°C (Kuo
et al., 2001). Yellow-spring effluents have a very low
pH (as low as 1.52) and a wide range of chemical
compositions. White-spring effluents are character-
ized by relatively low concentrations of copper, iron,
and methane (Chen et al., 2005a). The hydrothermal
fluids reach their highest temperatures about 3.5 h
after each high tide. The effluents from the vents
emerge to the sea surface and are then transported and
mixed by tidal movements (Chen et al., 2005b). Gases
produced here at the vent sites are mainly composed of
carbon dioxide and a small amount of hydrogen sulfide
(Tang et al., 2013). The hydrothermal mineralization
products at the Kueishantao vent field are mostly
sulfur-forming chimneys, mounds, and sedimentary
balls (Hwang & Lee, 2003; Zeng et al., 2011).
Metagenomic characterization of the bacterial com-
munities at the vent smokers and the surface waters of
Kueishantao has revealed a high abundance of
chemosynthetic bacteria (Tang et al., 2013; Wang
et al., 2015). Like in most shallow-water vent ecosys-
tems, energy is supplied here by both photosynthesis
and chemosynthesis (Jeng et al., 2004). The macro-
fauna at Kueishantao is characterized by vent crabs,
sea anemones, gobies, sessile algae, mollusks, and sea
snakes (Hwang & Lee, 2003). These organisms are
commonly seen in the surroundings of the vents in low
abundances and their life histories are highly affected
by vent eruptions (Peng et al., 2011; Dahms et al.,
2013,2014a,b). In shallow-water HVs, species
richness is commonly positively correlated with
distance from the HVs (Zeppilli & Danovaro, 2009).
The influence of the vent decreases with increasing
horizontal distance because of the dilution and lower
concentration of toxicants by sea water (Melwani &
Kim, 2008). However, previous studies at shallow-
water HVs commonly considered only small spatial
scales around the vents and are limited in reflecting the
range influenced by HVs (Tarasov et al., 1999).
When comparing deep sea and shallow-water sites,
there are inherent environmental stress differences
between the two environments (Table 1). Hydrostatic
pressure is one of the most important parameter that
was distinguishing deep sea from shallower waters
(Siebenaller, 2000) and HVs accordingly. Shallow-
water organisms have to cope with more hydrody-
namic stress than organisms from deeper water
(Nielsen et al., 2017) and their HVs.
Chan et al. (2014) investigated the response of
metal accumulation in the coral Tubastraea coccinea
from several environments such as from the Kueis-
hantao HVs. Metal accumulation was found substan-
tially higher in the tissues than in the skeletons. The
metals yielded differential amounts between skeletons
and tissues indicating that such coral had a distinct
selectivity for assimilating metals from seawater. The
above study indicates that metal accumulation in
skeletons and tissues represents a suitable instrument
for monitoring long-term effects of corals in various
polluted environments. However, tissues were more
sensitive than skeletons. We may conclude that
shallow HVs can be used as ‘‘natural laboratories’’
to assess the effects of climate change.
Conclusions
Easily accessible shallow HVs pose important advan-
tages for experimental possibilities to researchers
using genomic methods since it is feasible to perform
short-term and long-term experiments regarding the
genomic effects of low pH and temperature in
organisms from HVs. They can be used as natural
laboratories to assess the effects of global climate
change. Time of collection to preservation is mini-
mized in shallow HVs and high-quality DNA/RNA, a
prerequisite for genomic studies, can be routinely
extracted from the organisms. Caution should be used
when relating biological changes along pH gradients
to the direct effect of pH, as interactions with multiple
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123

stressors, including trace element enrichments, may be
present at the same time. The combination of stressful
physical and chemical factors and elevated element
concentrations in sediments and seawater may create a
harmful environment for most marine biota. HVs may
be considered as analogues for low pH environments
with non-negligible trace element contamination,
which in a scenario of continuous anthropogenic
impact, may become a common global change issue.
In situ studies are of particular importance and
interest in the era of genomics and next-generation
sequencing (NGS) methods. NGS techniques require
high-quality DNA and RNA templates and this is
technically difficult and expensive with deep HV
animals since substantial time passes from the collec-
tion of animals to the flash-freezing of tissues. During
this time, the quality of DNA and particularly RNA
may degrade significantly, rendering RNA-seq or
other transcriptomic studies of limited use. Gene
expression (RNA-seq), proteomics, metabolomics-
based experiments require an instant cessation of all
cellular activities in order to provide an accurate
profile of the gene expression, as well as proteomic
and metabolic activities. Access to a shallow-water
HV system provides researchers with the opportunity
of designing robust genome-based experiments with
no compromise on the tissue quality. The reduction of
cost and accessibility of shallow HVs also allows
long-term monitoring experiments with frequent
observations. Sudden changes in chemistry and/or
geology can quickly be monitored and opportunistic
experiments with the resident fauna can be conducted.
Such quick responses are next to impossible in deep
HVs. Of particular interest are the following OMICs-
based questions regarding HV animals and microor-
ganisms: (1) comparison of transcriptomic profiles
between resident and non-resident biota but phyloge-
netically related fauna to test for genes related to
habitat adaptations; (2) comparison of transcriptomic
profiles of resident fauna at different distances from
the vents to test the amount of variability of gene
expression in different combinations of pH and
temperature; (3) metagenomic studies of benthic and
water column bacterial communities inhabiting the
HVs to compare the microbial diversity of HVs
compared to those at different distances from the
vents; (4) community transcriptomics which may
reveal universal patterns of protein sequence conser-
vation in natural HV microbial communities versus
those found further away from the vents; (5) commu-
nity proteomics and metabolomics.
Acknowledgements We are grateful for the funding by the
Ministry of Science and Technology, Taiwan from projects
(Grant No. MOST 103-2611-M-019-002, MOST 104-2621-M-
019-002, MOST 104-2611-M-019-004, MOST 105-2621-M-
019-001, MOST 105-2621- M-019-002 and MOST 106-2621-
M-019-001) to J. S. Hwang. We further acknowledge funding
through MOST 104-2621-M-037-001 and MOST 105-2621-M-
037-001 to T. H. Shih. This work was partly supported by a grant
from the Research Center for Environmental Medicine,
Kaohsiung Medical University (KMU-TP105A27) to H.U.D.
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