Osmoregulatory evolution of gills promoted salinity adaptation following the sea–land transition of crustaceans

Hongguang Liu , Xiaokun Wang , Zeyu Liu , Shuqiang Li , Zhonge Hou

Marine Life Science & Technology ›› 2025, Vol. 7 ›› Issue (2) : 205 -217.

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Marine Life Science & Technology ›› 2025, Vol. 7 ›› Issue (2) : 205 -217. DOI: 10.1007/s42995-025-00298-6
Research Paper

Osmoregulatory evolution of gills promoted salinity adaptation following the sea–land transition of crustaceans

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Abstract

The sea–land transition is one of the most dramatic evolutionary changes and requires an adaptive genetic response to salinity changes and osmotic stress. Here, we used multi-species genomes and multi-tissue transcriptomes of the talitrid crustaceans, a living sea–land transition model, to investigate the adaptive genetic changes and osmoregulatory organs that facilitated their salinity adaptation. Genomic analyses detected numerous osmoregulatory genes in terrestrial talitrids undergoing gene family expansions and positive selection. Gene expression comparisons among species and tissues confirmed the gill being the primary organ responsible for ion transport and identified the genetic expression variation that enable talitrids to adapt to marine and land habitats. V-type H+-ATPases related to H+ transport play a crucial role in land adaptations, while genes related to the transport of inorganic ions (Na+, K+, Cl) are upregulated in marine habitats. Our results demonstrate that talitrids have divergent genetic responses to salinity change that led to the uptake or excretion of ions in the gills and promoted habitat adaptation. These findings suggest that detecting gene expression changes in talitrids presents promising potential as a biomarker for salinity monitoring.

Keywords

Genetic adaptation / Gill / Habitat transition / Ion transport / Biological Sciences / Genetics

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Hongguang Liu, Xiaokun Wang, Zeyu Liu, Shuqiang Li, Zhonge Hou. Osmoregulatory evolution of gills promoted salinity adaptation following the sea–land transition of crustaceans. Marine Life Science & Technology, 2025, 7(2): 205-217 DOI:10.1007/s42995-025-00298-6

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References

[1]

AlongeM, LebeigleL, KirscheM, JenikeK, OuS, AganezovS, WangX, LippmanZ, SchatzMC, SoykS. Automated assembly scaffolding using RagTag elevates a new tomato system for high-throughput genome editing. Genome Biol, 2022, 23: 258.

[2]

BröerS, GetherU. The solute carrier 6 family of transporters. Brit J Pharmacol, 2012, 167: 256-278.

[3]

BrooksSJ, MillsCL. Gill Na+, K+-ATPase in a series of hyper-regulating gammarid amphipods. Enzyme characterisation and the effects of salinity acclimation. Comp Biochem Physiol Part A: Mol Integr Physiol, 2006, 144: 24-32.

[4]

BuD, LuoH, HuoP, WangZ, ZhangS, HeZ, WuY, ZhaoL, LiuJ, GuoJ, FangS, CaoW, YiL, ZhaoY, KongL. KOBAS-i: intelligent prioritization and exploratory visualization of biological functions for gene enrichment analysis. Nucleic Acids Res, 2021, 49: W317-W325.

[5]

CannizzaroAG, BergDJ. Gone with Gondwana: amphipod diversification in freshwaters followed the breakup of the supercontinent. Mol Phylogenet Evol, 2022, 171. 107464

[6]

CuiZ, LiuY, YuanJ, ZhangX, VenturaT, MaKY, SunS, SongC, ZhanD, YangY, LiuH, FanG, CaiQ, DuJ, QinJ, ShiC, HaoS, FitzgibbonQP, SmithGG, XiangJ, et al. . The Chinese mitten crab genome provides insights into adaptive plasticity and developmental regulation. Nat Commun, 2021, 12: 2395.

[7]

De BieT, CristianiniN, DemuthJP, HahnMW. CAFE: a computational tool for the study of gene family evolution. Bioinformatics, 2006, 22: 1269-1271.

[8]

EmmsDM, KellyS. OrthoFinder: phylogenetic orthology inference for comparative genomics. Genome Biol, 2019, 20: 1-14.

[9]

FriendJA, RichardsonAM. Biology of terrestrial amphipods. Annu Rev Entomol, 1986, 31: 25-48.

[10]

HänzelmannS, CasteloR, GuinneyJ. GSVA: gene set variation analysis for microarray and RNA-seq data. BMC Bioinform, 2013, 14: 1-15.

[11]

HenriquezT, WirtzL, SuD, JungH. Prokaryotic solute/sodium symporters: versatile functions and mechanisms of a transporter family. Int J Mol Sci, 2021, 22: 1880.

[12]

HenryRP, LucuČ, OnkenH, WeihrauchD. Multiple functions of the crustacean gill: osmotic/ionic regulation, acid-base balance, ammonia excretion, and bioaccumulation of toxic metals. Front Physiol, 2012, 3: 431.

[13]

JeongH, MasonSP, BarabásiAL, OltvaiZN. Lethality and centrality in protein networks. Nature, 2001, 411: 41-42.

[14]

KirschnerLB. The mechanism of sodium chloride uptake in hyperregulating aquatic animals. J Exp Biol, 2004, 207: 1439-1452.

[15]

Kryuchkova-MostacciN, Robinson-RechaviM. A benchmark of gene expression tissue-specificity metrics. Brief Bioinform, 2017, 18: 205-214

[16]

LangfelderP, HorvathS. WGCNA: an R package for weighted correlation network analysis. BMC Bioinform, 2008, 9: 1-13.

[17]

LeeCE. Ion transporter gene families as physiological targets of natural selection during salinity transitions in a copepod. Physiology, 2021, 36: 335-349.

[18]

LeeCE, KiergaardM, GelembiukGW, EadsBD, PosaviM. Pumping ions: rapid parallel evolution of ionic regulation following habitat invasions. Evolution, 2011, 65: 2229-2244.

[19]

LeekJT, JohnsonWE, ParkerHS, JaffeAE, StoreyJD. The sva package for removing batch effects and other unwanted variation in high-throughput experiments. Bioinformatics, 2012, 28: 882-883.

[20]

LiB, DeweyCN. RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinform, 2011, 12: 1-16.

[21]

LiD, LiuCM, LuoR, SadakaneK, LamTW. MEGAHIT: an ultra-fast single-node solution for large and complex metagenomics assembly via succinct de Bruijn graph. Bioinformatics, 2015, 31: 1674-1676.

[22]

LiuH, TongY, ZhengY, LiS, HouZ. Sea–land transition drove terrestrial amphipod diversification in East Asia, with a description of a new species. Zool J Linn Soc-London, 2022, 196: 940-958.

[23]

LiuH, ZhengY, ZhuB, TongY, XinW, YangH, JinP, HuY, HuangM, ChangWJ, BallarinF, LiS, HouZ. Marine-montane transitions coupled with gill and genetic convergence in extant crustacean. Sci Adv, 2023, 9: eadg4011.

[24]

LoveMI, HuberW, AndersS. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol, 2014, 15: 1-21.

[25]

LucuČ, TowleDW. Na++K+-ATPase in gills of aquatic crustacea. Comp Biochem Physiol Part A: Mol Integr Physiol, 2003, 135: 195-214.

[26]

MaraschiAC, FariaSC, McNamaraJC. Salt transport by the gill Na+-K+-2Cl symporter in palaemonid shrimps: exploring physiological, molecular and evolutionary landscapes. Comp Biochem Physiol Part A: Mol Integr Physiol, 2021, 257. 110968

[27]

McNamaraJC, FariaSC. Evolution of osmoregulatory patterns and gill ion transport mechanisms in the decapod Crustacea: a review. J Comp Physiol, 2012, 182: 997-1014.

[28]

Moreno-HagelsiebG, LatimerK. Choosing BLAST options for better detection of orthologs as reciprocal best hits. Bioinformatics, 2008, 24: 319-324.

[29]

PochynyukO, StockandJD, StaruschenkoA. Ion channel regulation by Ras, Rho, and Rab small GTPases. Exp Biol Med, 2007, 232: 1258-1265.

[30]

RitchieME, PhipsonB, WuDI, HuY, LawCW, ShiW, SmythGK. limma powers differential expression analyses for RNA-sequencing and microarray studies. Nucleic Acids Res, 2015, 43. e47

[31]

SandersonMJ. r8s: inferring absolute rates of molecular evolution and divergence times in the absence of a molecular clock. Bioinformatics, 2003, 19: 301-302.

[32]

SpicerJI, MoorePG, TaylorAC. The physiological ecology of land invasion by the Talitridae (Crustacea: Amphipoda). P Roy Soc B-Biol Sci, 1987, 232: 95-124

[33]

SteineggerM, SödingJ. MMseqs2 enables sensitive protein sequence searching for the analysis of massive data sets. Nat Biotech, 2017, 35: 1026-1028.

[34]

SternDB, LeeCE. Evolutionary origins of genomic adaptations in an invasive copepod. Nat Ecol Evol, 2020, 4: 1084-1094.

[35]

SwainR, RichardsonAM. An examination of gill area relationships in an ecological series of talitrid amphipods from Tasmania (Amphipoda: Talitridae). J Nat Hist, 1993, 27: 285-297.

[36]

ThabetR, AyadiH, KokenM, LeignelV. Homeostatic responses of crustaceans to salinity changes. Hydrobiologia, 2017, 799: 1-20.

[37]

TowleDW, KaysWT. Basolateral localization of Na+ + K+-ATPase in gill epithelium of two osmoregulating crabs, Callinectes sapidus and Carcinus maenas. J Exp Zool, 1986, 239: 311-318.

[38]

TsaiJR, LinHC. V-type H+-ATPase and Na+, K+-ATPase in the gills of 13 euryhaline crabs during salinity acclimation. J Exp Biol, 2007, 210: 620-627.

[39]

WangK, WangJ, ZhuC, YangL, RenY, RuanJ, FanG, HuJ, XuW, BiX, ZhuY, SongY, ChenH, MaT, ZhaoR, JiangH, ZhangB, FengC, YuanY, GanX, et al. . African lungfish genome sheds light on the vertebrate water-to-land transition. Cell, 2021, 184: 1362-1376.

[40]

Watson-ZinkVM. Making the grade: physiological adaptations to terrestrial environments in decapod crabs. Arthropod Struct Dev, 2021, 64. 101089

[41]

WeihrauchD, ZieglerA, SiebersD, TowleD. Molecular characterization of V-type H (+)-ATPase (B-subunit) in gills of euryhaline crabs and its physiological role in osmoregulatory ion uptake. J Exp Biol, 2001, 204: 25-37.

[42]

WuT, HuE, XuS, ChenM, GuoP, DaiZ, FengT, ZhouL, TangW, ZhanL, FuX, LiuS, BoX, YuG. Cluster profiler 40: a universal enrichment tool for interpreting omics data. The Innovation, 2021, 2: 100141.

[43]

YangZ. PAML 4: phylogenetic analysis by maximum likelihood. Mol Bio Evol, 2007, 24: 1586-1591.

[44]

YangL, HouZ, LiS. Marine incursion into East Asia: a forgotten driving force of biodiversity. Proc R Soc B Biol Sci, 2013, 280: 20122892.

[45]

YaoH, LiX, ChenY, LiangG, GaoG, WangH, WangC, MuC. Metabolic changes in Scylla paramamosain during adaptation to an acute decrease in salinity. Front Mar Sci, 2021, 8. 734519

[46]

YuG, LiF, QinY, BoX, WuY, WangS. GOSemSim: an R package for measuring semantic similarity among GO terms and gene products. Bioinformatics, 2010, 26: 976-978.

[47]

YuanJ, ZhangX, LiuC, DuanH, LiF, XiangJ. Convergent evolution of the osmoregulation system in decapod shrimps. Mar Biotechnol, 2017, 19: 76-88.

[48]

YuanJ, ZhangX, WangM, SunY, LiuC, LiS, YuY, GaoY, LiuF, ZhangX, KongJ, FanG, ZhangC, FengL, XiangJ, LiF. Simple sequence repeats drive genome plasticity and promote adaptive evolution in penaeid shrimp. Commun Biol, 2021, 4: 186.

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