Adaptive mechanisms for cold temperature
A good understanding of how ecological variants of fishes can affect
their population structure will provide more comprehensive implications
for conservation management and decision-making (Li, Xue, Zhang, & Liu,
2018). Water temperature is one of the most important abiotic factors
that influence the phenotypes and habitats of aquatic organisms (Chen,
Farrell, Matala, Hoffman, & Narum, 2018). As an important environmental
stressor, low and high temperatures have broad biological effects on
marine organisms. These thermal effects generate intense selective
pressures on several genes and genome regions.
In this study, selective sweep was conducted to identify the thermally
affected genes between the northern and southern populations of S.
japonica . The strategy of combining alternative statistical approaches
in detecting selective signatures can provide sound results by
decreasing false-positive rates. We evaluated the genetic attributes of
the candidate genes relative to the genomic background. We scanned the
genome-wide variations using F ST and π ratio
values. The cold- and high-temperature adaptation conditions shared only
two candidate genes.
A total of 81 candidate genes shared by both the π ratio andF ST analysis in the RS population were recognized
as potentially affected genes related to cold adaptation. Cold
adaptation and acclimatization studies suggested that more than
one mechanism is involved in the
biological response to cold stress (White, Alton, & Frappell, 2012; Liu
et al., 2018). Consistent with our expectations from the biological
complexity of cold adaptation, several different processes, rather than
one particular term or pathway, were highlighted by our selection tests.
Low temperatures may influence energy metabolism. Nine selection genes
(low-density lipoprotein receptor [LDLR ], ZBTB20 ,PICALM , and nup35 ) were related to lipid metabolic
process. Lipids are the main components of cytomembrane (Meer, Voelker,
& Feigenson, 2008). A common cold adaptation mechanism for the cell is
to manipulate the membrane lipid composition to maintain membrane
fluidity and, correspondingly, proper membrane permeability and function
of membrane protein complexes (e.g., transporters) (Russell &Nichols,
1999).
Previous studies showed that the permeability of cell membranes
considerably changes under long-term low temperature conditions and
damages the integrity and stability of cell membranes. The LDLRgene is one important candidate gene for cold adaptation. LDLR , a
glycoprotein located on the surface of cells, mediates the endocytic
uptake of LDL cholesterol in the liver, which is a key regulator of the
metabolism of plasma low-density lipoprotein cholesterol. LDLR is the most powerful determinant of variation in
total cholesterol and LDL cholesterol levels (Hansen et al., 1997). This
gene plays an essential role in protecting cell membrane integrity under
cold stress. The strong selection pressure on this gene is useful in
adapting to low temperatures. A similar result was also observed in the
low-density lipoprotein receptor-related protein 5 (LRP5 ) gene,
another gene member of low-density lipoprotein receptor of humans
(Cardona et al., 2014). LRP5 shows strong signals of selection in
indigenous Siberian human populations. LRP5 has a high expression
in the liver of humans and plays a role in cholesterol metabolism.
Natural selection of the LRP5 gene helps Siberian persons to cope
with the cold climate. The TPO gene is involved in thyroid
metabolism (Leonard, Snodgrass, & Sorensen, 2005). The thyroid
determines the basal metabolic rate of the body. Natural selection of
the TPO gene in the RS population may maintain the basal
metabolic rate and stabilize lipid levels in the serum.
We also detected substantial adaptive evidence concerning ion exchange
and transportation, which are processes that affect the fluidity and
permeability of the cell membrane and directly and indirectly linked to
thermal regulation. We identified a considerable
number of genes that encode transporters (the MFS transportersSLC22A5 , SLC7A2 , and SLC25A5 ) and ion channels
(e.g., the voltage-gated sodium channel SCN4B ) in the genome
regions of the RS population under selective sweeps. For example,SLC22A5 is a specific transporter that exists in the membranes of
cells and mitochondria involved in the uptake or release of carnitine.
Four copies of SLC22A5 in the genome of S. japonicaindicated gene expansion. Carnitine is a carrier for long-fatty acids
and facilitates their transport into the mitochondria for lipid
oxidation. Defective SLC22A5 causes systemic carnitine
deficiency, resulting in metabolic decompensation. SLC7A2functions as a permease involved in transporting cationic amino acids
across the plasma membrane. These transporter and ion channel genes are
crucial for transmembrane transport to maintain a stable balance between
the internal and external environments of cells under cold temperature.
Therefore, the genes that encode transcellular ion transporters and
channel proteins are reshaped by natural selection under cold stress
environment.
Smooth muscle contraction, which includes vasoconstriction and
vasodilation, is another process implicated in cold adaptation. Two
genes involved in this process that showed evidence of strong signals of
selection are CPI17 (protein phosphatase 1 regulatory subunit
14A) and CACNB4 . CPI17 is the inhibitor of PPP1CA. It has
more than 1000-fold inhibitory activity when phosphorylated, creating a
molecular switch for regulating the phosphorylation status of PPP1CA
substrates and smooth muscle contraction in the absence of increased
intracellular Ca2+ concentration (Li et al., 2001).
The CACNB4 gene encodes a calcium channel subunit expressed in
the heart and increases peak calcium current that is important for
cardiac muscle contraction under cold stress (Rouhiainen et al., 2016).
Although no data on the heart rate of the populations are available,
cold exposure is known to increase cardiac pressure. Thus, this
efficient cardiovascular regulation might be a possible cold adaptive
mechanism in the RS population. These genetic changes might facilitate
the adaptation and survival of S. japonica in low-temperature
areas.
Cell repair and clear necrotic organelles are also important processes
of cold adaptation in the RS population. Interferon regulatory factor 1
(IRF1 ) is a transcriptional regulator that displays a remarkable
functional diversity in regulating cellular responses (Oshima et al.,
2004). Under cold stress, IRF1 causes cells to suspend
proliferation to survive in adverse environmental conditions and also
decisively triggers apoptosis when cell damage becomes irreparable,
thereby preventing harmful cells from harming other normal cells. DnaJ
homolog subfamily C member 10 is involved in the correct folding of
proteins and the degradation of misfolded proteins (Oka, Pringle,
Schopp, Braakman, & Bulleid, 2013). It promotes the apoptotic signaling
pathway in response to endoplasmic reticulum stress.
The enrichment tests provided 50 significant GO terms and one KEGG
pathway after FDR adjustment. The enrichment GO categories and KEGG
pathways were primarily associated with cell apart, transmembrane
transporter activity, tissue homeostasis, lipid metabolism, apoptosis,
and vascular smooth muscle contraction. These functional clusters are
biologically relevant to cold adaptations and essential in regulating
mechanisms for fish to respond to a cold environment.