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Gill Transcriptome Analysis Revealed the Difference in Gene Expression Between Freshwater and Seawater Acclimated Guppy (Poecilia reticulata)

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Abstract

Guppy (Poecilia reticulata) can adapt to a wide range of salinity changes. To investigate the gene expression changes in the guppy exposed to seawater, we characterized its gill transcriptome using RNA sequencing. Experimental fish were exposed to salinity increase from 0 to 30‰ within 4 days, while control fish were cultured in freshwater (0‰ salinity). Seven days after salinity exposure, the gills were sampled and the mortality within 2 weeks was recorded. No significant difference in the cumulative mortality at the second week was found between the two groups. Transcriptomic analysis identified 3477 differentially expressed genes (DEGs), including 1067 upregulated and 2410 downregulated genes. These DEGs were enriched in several biological processes, including ion transport, ion homeostasis, ATP biosynthetic process, metabolic process, and immune system process. Oxidative phosphorylation was the most activated pathway. DEGs involved in the pathway “endoplasmic reticulum (ER)-mediated phagocytosis,” “starch and sucrose metabolism,” and “steroid biosynthesis” were mainly downregulated; chemokines and interleukins involved in “cytokine-cytokine receptor interaction” were differentially expressed. The present results suggested that oxidative phosphorylation had essential roles in osmoregulation in the gills of seawater acclimated guppy, during which the decline in the expression of genes encoding V-ATPases and calreticulin had a negative effect on the phagocytosis and immune response. Besides, several metabolic processes including “starch and sucrose metabolism” and “steroid biosynthesis” were affected. This study elucidates transcriptomic changes in osmotic regulation, metabolism, and immunity in seawater acclimated guppy.

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Data Availability

All the data supporting our findings are contained within the manuscript. The raw sequence data generated from this study have been deposited in the Genome Sequence Archive (GSA) database in the BIG Data Center (http://gsa.big.ac.cn/index.jsp) under the accession number CRA002620 and will be made publicly available upon acceptance of this manuscript for publishing. Shared URL: https://ngdc.cncb.ac.cn/gsa/s/BBfv9BLi

Abbreviations

act-1a :

Actinidain

actbb :

Actin, cytoplasmic 2

acvr1 :

Activin receptor type-1

amh :

Anti-Müllerian hormone

amy1 :

Alpha-amylase 1

amy2 :

Pancreatic alpha-amylase

ATP:

Adenosine triphophate

atp1a1 :

ATPase Na + /K + transporting subunit alpha 1

atp5f1a :

ATP synthase F1 subunit alpha

atp5o :

ATP synthase subunit O

atp6v1a :

V-type proton ATPase catalytic subunit A

atp6v1b2 :

V-type proton ATPase subunit B, brain isoform

atp6v1e1 :

V-type proton ATPase subunit E 1

BP:

Biological process

ca1 :

Carbonic anhydrase 1

calr :

Calreticulin

CC:

Cellular component

ccl19 :

C-C chemokine ligand 19

ccl20 :

C-C chemokine ligand 20

ccl21 :

C-C chemokine ligand 21

ccl4 :

C-C motif chemokine ligand 4

ccr4 :

C-C chemokine receptor type 4

ccr6 :

C-C chemokine receptor type 6

cDNA:

Complementary DNA

cftr :

Cystic fibrosis transmembrane conductance regulator

cox4i1 :

Cytochrome C oxidase subunit IV isoform 1

cox5a :

Cytochrome c oxidase subunits Va

Ct:

Cycle threshold

ctsl :

Procathepsin L

cyia :

Actin, cytoskeletal 1A

cyp24a1 :

Cytochrome P450 family 24 subfamily A member 1

cyp2r1 :

Cytochrome P450 family 2 subfamily R member 1

cyp51a1 :

Cytochrome P450 family 51 subfamily A member 1

DEGs:

Differentially expressed genes

ebp :

Emopamil-binding protein

edar :

Ectodysplasin A receptor

enpp3 :

Ectonucleotide pyrophosphatase/ phosphodiesterase 3

ER:

Endoplasmic reticulum

faxdc2 :

Fatty acid hydroxylase domain containing 2

FC:

Fold change

FDR:

False discovery rate

g6pc :

Glucose-6-phosphatase

gapdh :

Glyceraldehyde-3-phosphate dehydrogenase

gck :

Glucokinase

Gh/Igf1:

Growth hormone/insulin growth factor-1

GO:

Gene ontology

gpi :

Glucose phosphate isomerase

GSA:

Genome Sequence Archive

gys2 :

Glycogen synthase 2

h2-aa :

H-2 class II histocompatibility antigen, A-U alpha chain

h2-eb1 :

Ig-like domain-containing protein

h2-t23 :

H-2 class I histocompatibility antigen, D-37 alpha chain

hla-c :

Human leukocyte antigen class I C

hla-dpa1 :

HLA Class II histocompatibility antigen, DP alpha 1 chain

hla-dra :

HLA Class II histocompatibility antigen, DR alpha chain

hsd17b7 :

17-Beta-hydroxysteroid dehydrogenase 7

ifnar2 :

Interferon alpha/beta receptor 2

il-1 :

Interleukin-1

il10 :

Interleukin-10

il10ra :

Interleukin 10 receptor subunit alpha

il11 :

Interleukin-11

il12 :

Interleukin-12

il12rb2 :

Interleukin 12 receptor beta 2

il-17 :

Interleukin-17

il17rb :

Interleukin 17 receptor beta

il1b :

Interleukin 1, beta

il1r2 :

Interleukin 1 receptor type 2

il1rap :

Interleukin 1 receptor accessory protein

il20rb :

Interleukin 20 receptor beta

il26 :

Interleukin-26

il8 :

Interleukin-8

iTRAQ:

Isobaric tags for relative and absolute quantification

KEGG:

Kyoto encyclopedia of genes and genomes

kita:

Tyrosine-protein kinase kit

lss :

Lanosterol synthase

lta :

Lymphotoxins A

ltbr :

Lymphotoxin-beta receptor

MF:

Molecular function

mgam :

Maltase-glucoamylase

MHC-I:

Major histocompatibility complex class I

MHC-II:

Major histocompatibility complex class II

mpo :

Myeloperoxidase

mr1 :

MHC-related protein 1

mx:

Myxovirus resistance

NADH:

Nicotinamide adenine dinucleotide

ndufa1 :

NADH dehydrogenase (ubiquinone) 1 alpha subcomplex 1

ndufa4 :

NADH dehydrogenase (ubiquinone) 1 alpha subcomplex subunit 4

ndufs1 :

NADH dehydrogenase (ubiquinone) Fe-S protein 1

ndufv1 :

NADH dehydrogenase ubiquinone flavoprotein

nos1 :

Nitric oxide synthase

nsdhl :

Sterol-4-alpha-carboxylate 3-dehydrogenase, decarboxylating

odc1 :

Ornithine decarboxylase 1

PDGF:

Platelet-derived growth factor

pgm1 :

Phosphoglucomutase-1

pygl :

Glycogen phosphorylase, liver form

pH:

Potential of hydrogen

prl :

Prolactin

pygm :

Glycogen phosphorylase, muscle form

qPCR:

Quantitative real-time PCR

RIN:

RNA integrity number

RNA-seq:

High-throughput RNA sequencing

ROS:

Reactive oxygen species

rt1-b :

RT1 class II histocompatibility antigen

RT-PCR:

Reverse transcription polymerase chain reaction

scn1b :

Sodium voltage-gated channel beta subunit 1

sec61a :

Protein transport protein sec61 subunit alpha

slc4a4 :

Sus scrofa domestica sodium bicarbonate cotransporter member 4

slc9a2 :

Solute carrier family 9 (sodium/hydrogen exchanger), member 2

slc12a2 :

Solute carrier family 12 member 2

slc12a3 :

Solute carrier family 12 member 3

slc13a1 :

Solute carrier family 13 member 1

soat1 :

Sterol O-acyltransferase 1

SPSS:

Statistical product and service solutions

tcirg1 :

T-cell immune regulator 1

TGF-β:

Transforming growth factor-β

tm7sf2 :

Transmembrane 7 superfamily member 2

TNF:

Tumor necrosis factor

treh :

Trehalase

trpv4 :

Transient receptor potential cation channel subfamily V member 4

ugp2 :

UTP-glucose-1-phosphate uridylyltransferase

ugt1a1 :

UDP glucuronosyltransferase family 1 member A1

ugt1a5 :

UDP glucuronosyltransferase family 1 member A5

ugt2a1 :

UDP glucuronosyltransferase family 2 member A1

ugt2a2 :

UDP glucuronosyltransferase family 2 member A2

ugt2a3 :

UDP glucuronosyltransferase family 2 member A3

uqcrfs1 :

Ubiquinol-cytochrome C reductase iron-sulfur subunit 1

uqcrh :

Ubiquinol-cytochrome c reductase hinge protein

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Funding

This study was supported by Fujian Provincial Department of Science and Technology (Grant No. 2015R1019-13, 2018R1019-6), and General Projects of Fujian Academy of Agricultural Science (AC2017-1).

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Authors and Affiliations

  1. Biotechnology Institute, Fujian Academy of Agricultural Sciences, Fuzhou, China

    Xiuxia Chen, Hui Gong, Hongshu Chi, Binfu Xu & Zaiyu Zheng

  2. State Key Laboratory of Marine Environmental Science, College of Ocean and Earth Sciences, Xiamen University, Xiamen, China

    Yulin Bai

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  1. Xiuxia Chen
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Contributions

HG conceived and supervised the study. XC wrote the manuscript. XC and HC conducted the salinity challenge experiment. XC and HG performed the analysis and designed the charts and tables. XC and BX extracted total RNA from the gill tissues. XC, HC, BX, and ZZ collected the samples. HG and XC revised the manuscript. YB participated in PPI analysis. All the authors have read and approved the manuscript.

Corresponding author

Correspondence to Hui Gong.

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The Research Ethics Committee of Fujian Academy of Agricultural Sciences approved the study. All experimental fish procedures were performed in accordance with the regulations for the Administration of Affairs Concerning Experimental Animals, approved by the State Council of China.

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Chen, X., Gong, H., Chi, H. et al. Gill Transcriptome Analysis Revealed the Difference in Gene Expression Between Freshwater and Seawater Acclimated Guppy (Poecilia reticulata). Mar Biotechnol 23, 615–627 (2021). https://doi.org/10.1007/s10126-021-10053-4

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