Insights into the strategy of micro-environmental adaptation: Transcriptomic analysis of two alvinocaridid shrimps at a hydrothermal vent

Autoři: Fang-Chao Zhu aff001;  Jin Sun aff003;  Guo-Yong Yan aff001;  Jiao-Mei Huang aff001;  Chong Chen aff004;  Li-Sheng He aff001
Působiště autorů: Institute of Deep-sea Science and Engineering, Chinese Academy of Sciences, Sanya, Hainan, China aff001;  College of Earth and Planetary Sciences, University of Chinese Academy of Sciences, Beijing, China aff002;  Department of Ocean Science, The Hong Kong University of Science and Technology, Hong Kong, China aff003;  Japan Agency for Marine-Earth Science and Technology (JAMSTEC), Yokosuka, Kanagawa, Japan aff004
Vyšlo v časopise: PLoS ONE 15(1)
Kategorie: Research Article
doi: 10.1371/journal.pone.0227587


Diffusing fluid at a deep-sea hydrothermal vent creates rapid, acute physico-chemical gradients that correlate strongly with the distribution of the vent fauna. Two alvinocaridid shrimps, Alvinocaris longirostris and Shinkaicaris leurokolos occupy distinct microhabitats around these vents and exhibit different thermal preferences. S. leurokolos inhabits the central area closer to the active chimney, while A. longirostris inhabits the peripheral area. In this study, we screened candidate genes that might be involved in niche separation and microhabitat adaptation through comparative transcriptomics. The results showed that among the top 20% of overexpressed genes, gene families related to protein synthesis and structural components were much more abundant in S. leurokolos compared to A. longirostris. Moreover, 15 out of 25 genes involved in cellular carbohydrate metabolism were related to trehalose biosynthesis, versus 1 out of 5 in A. longirostris. Trehalose, a non-reducing disaccharide, is a multifunctional molecule and has been proven to act as a protectant responsible for thermotolerance in Saccharomyces cerevisiae. Putative positively selected genes involved in chitin metabolism and the immune system (lectin, serine protease and antimicrobial peptide) were enriched in S. leurokolos. In particular, one collagen and two serine proteases were found to have experienced strong positive selection. In addition, sulfotransferase-related genes were both overexpressed and positively selected in S. leurokolos. Finally, genes related to structural proteins, immune proteins and protectants were overexpressed or positively selected. These characteristics could represent adaptations of S. leurokolos to its microhabitat, which need to be confirmed by more evidence, such as data from large samples and different development stages of these alvinocaridid shrimps.

Klíčová slova:

Hydrothermal vents – Lectins – Multiple alignment calculation – Sequence alignment – Sequence databases – Serum proteins – Shrimp – Transcriptome analysis


1. Pedersen RB, Rapp HT, Thorseth IH, Lilley MD, Barriga FJ, Baumberger T, et al. Discovery of a black smoker vent field and vent fauna at the Arctic Mid-Ocean Ridge. Nat Commun. 2010; 1: 126. doi: 10.1038/ncomms1124 21119639

2. Kelly N, Metaxas A, Butterfield D. Spatial and temporal patterns of colonization by deep-sea hydrothermal vent invertebrates on the Juan de Fuca Ridge, NE Pacific. Aquat Biol. 2007; 1: 1–16.

3. Cuvelier D, Sarradin PM, Sarrazin J, Colaço A, Copley JT, Desbruyères D, et al. Hydrothermal faunal assemblages and habitat characterisation at the Eiffel Tower edifice (Lucky Strike, Mid-Atlantic Ridge). Mar Ecol. 2011; 32(2): 243–255.

4. Husson B, Sarradin PM, Zeppilli D, Sarrazin J. Picturing thermal niches and biomass of hydrothermal vent species. Deep Sea Res Part 2 Top Stud Oceanogr. 2017; 137: 6–25.

5. Komai T, Segonzac M. A revision of the genus Alvinocaris Williams and Chace (Crustacea: Decapoda: Caridea: Alvinocarididae), with descriptions of a new genus and a new species of Alvinocaris. J Nat Hist. 2005; 39(15): 1111–1175.

6. Watanabe H, Kojima S. Vent fauna in the Okinawa Trough. In: Ishibashi J, Okino K, Sunamura M, editors. Subseafloor biosphere linked to hydrothermal systems. Tokyo: Springer; 2015. p. 449–459.

7. Gebruk AV, Southward EC, Kennedy H, Southward AJ. Food sources, behaviour, and distribution of hydrothermal vent shrimps at the Mid-Atlantic Ridge. J Mar Biol Assoc U.K. 2000; 80(3): 485–499.

8. Cottin D, Shillito B, Chertemps T, Thatje S, Léger N, Ravaux J. Comparison of heat-shock responses between the hydrothermal vent shrimp Rimicaris exoculata and the related coastal shrimp Palaemonetes varians. J Exp Mar Bio Ecol. 2010; 393(1–2): 9–16.

9. Hui M, Cheng J, Sha Z. Adaptation to the deep-sea hydrothermal vents and cold seeps: insights from the transcriptomes of Alvinocaris longirostris in both environments. Deep Sea Res Part 1 Oceanogr Res Pap. 2018; 135: 23–33.

10. Watanabe H, Yahagi T, Nagai Y, Seo M, Kojima S, Ishibashi J, et al. Different thermal preferences for brooding and larval dispersal of two neighboring shrimps in deep‐sea hydrothermal vent fields. Mar Ecol. 2016; 37(6): 1282–1289.

11. Vereshchaka AL, Kulagin DN, Lunina AA. Phylogeny and new classification of hydrothermal vent and seep shrimps of the family Alvinocarididae (Decapoda). PLoS One. 2015; 10(7): e0129975. doi: 10.1371/journal.pone.0129975 26161742

12. Gonzalez‐Rey M, Serafim A, Company R, Bebianno MJ. Adaptation to metal toxicity: a comparison of hydrothermal vent and coastal shrimps. Mar Ecol. 2010; 28(1): 100–107.

13. Gonzalez‐Rey M, Serafim A, Company R, Gomes T, Bebianno MJ. Detoxification mechanisms in shrimp: comparative approach between hydrothermal vent fields and estuarine environments. Mar Environ Res. 2008; 66(1): 35–37. doi: 10.1016/j.marenvres.2008.02.015 18405963

14. Cottin D, Ravaux J, Léger N, Halary S, Toullec JY, Sarradin PM, et al. Thermal biology of the deep-sea vent annelid Paralvinella grasslei: in vivo studies. J Exp Biol. 2008; 211: 2196–2204. doi: 10.1242/jeb.018606 18587113

15. Cottin D, Shillito B, Chertemps T, Tanguy A, Léger N, Ravaux J. Identification of differentially expressed genes in the hydrothermal vent shrimp Rimicaris exoculata exposed to heat stress. Mar Genomics. 2010; 3(2): 71–78. doi: 10.1016/j.margen.2010.05.002 21798199

16. Mestre NC, Cottin D, Bettencourt R, Colaço A, Correia SP, Shillito B, et al. Is the deep-sea crab Chaceon affinis able to induce a thermal stress response? Comp Biochem Physiol A Mol Integr Physiol. 2015; 181: 54–61. doi: 10.1016/j.cbpa.2014.11.015 25434602

17. Zhang J, Sun Q, Luan Z, Lian C, Sun L. Comparative transcriptome analysis of Rimicaris sp. reveals novel molecular features associated with survival in deep-sea hydrothermal vent. Sci Rep. 2017; 7: 2000. doi: 10.1038/s41598-017-02073-9 28515421

18. Wong YH, Sun J, He LS, Chen LG, Qiu JW, Qian PY. High-throughput transcriptome sequencing of the cold seep mussel Bathymodiolus platifrons. Sci Rep. 2015; 5: 16597. doi: 10.1038/srep16597 26593439

19. Zhang Y, Sun J, Chen C, Watanabe HK, Feng D, Zhang Y, et al. Adaptation and evolution of deep-sea scale worms (Annelida: Polynoidae): insights from transcriptome comparison with a shallow-water species. Sci Rep. 2017; 7: 46205. doi: 10.1038/srep46205 28397791

20. Fisher CR, Childress JJ, Arp AJ, Brooks JM, Distel D, Favuzzi JA, et al. Microhabitat variation in the hydrothermal vent mussel, Bathymodiolus thermophilus, at the Rose Garden vent on the Galapagos Rift. Deep Sea Res A. 1988; 35(10–11): 1769–1791.

21. Nakamura K, Kawagucci S, Kitada K, Kumagai H, Takai K, Okino K. Water column imaging with multibeam echo-sounding in the mid-Okinawa Trough: implications for distribution of deep-sea hydrothermal vent sites and the cause of acoustic water column anomaly. Geochem J. 2015; 49(6): 579–596.

22. Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics. 2014; 30(15): 2114–2120. doi: 10.1093/bioinformatics/btu170 24695404

23. Haas BJ, Papanicolaou A, Yassour M, Grabherr M, Blood PD, Bowden J, et al. De novo transcript sequence reconstruction from RNA-seq using the Trinity platform for reference generation and analysis. Nat Protoc. 2013; 8: 1494–1512. doi: 10.1038/nprot.2013.084 23845962

24. Simão FA, Waterhouse RM, Ioannidis P, Kriventseva EV, Zdobnov EM. BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs. Bioinformatics. 2015; 31(19): 3210–3212. doi: 10.1093/bioinformatics/btv351 26059717

25. Katoh K, Standley DM. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol. 2013; 30(4): 772–780. doi: 10.1093/molbev/mst010 23329690

26. Capella-Gutiérrez S, Silla-Martínez JM, Gabaldón T. TrimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics. 2009; 25(15): 1972–1973. doi: 10.1093/bioinformatics/btp348 19505945

27. Nguyen LT, Schmidt HA, von Haeseler A, Minh BQ. IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol Biol Evol. 2015; 32(1): 268–274. doi: 10.1093/molbev/msu300 25371430

28. Quevillon E, Silventoinen V, Pillai S, Harte N, Mulder N, Apweiler R, et al. InterProScan: protein domains identifier. Nucleic Acids Res. 2005; 33(suppl_2): W116–W120.

29. Conesa A, Götz S, García-Gómez JM, Terol J, Talón M, Robles M. Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics. 2005; 21(18): 3674–3676. doi: 10.1093/bioinformatics/bti610 16081474

30. Li B, Dewey CN. RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinformatics. 2011; 12: 323. doi: 10.1186/1471-2105-12-323 21816040

31. Ye J, Fang L, Zheng H, Zhang Y, Chen J, Zhang Z, et al. WEGO: a web tool for plotting GO annotations. Nucleic Acids Res. 2006; 34(suppl_2): W293–W297.

32. Remm M, Storm CE, Sonnhammer EL. Automatic clustering of orthologs and in-paralogs from pairwise species comparisons. J Mol Biol. 2001; 314(5): 1041–1052. doi: 10.1006/jmbi.2000.5197 11743721

33. Kersey PJ, Allen JE, Allot A, Barba M, Boddu S, Bolt BJ, et al. Ensembl Genomes 2018: an integrated omics infrastructure for non-vertebrate species. Nucleic Acids Res. 2018; 46(D1): D802–D808. doi: 10.1093/nar/gkx1011 29092050

34. Zhang Z, Xiao J, Wu J, Zhang H, Liu G, Wang X, et al. ParaAT: a parallel tool for constructing multiple protein-coding DNA alignments. Biochem Biophys Res Commun. 2012; 419(4): 779–781. doi: 10.1016/j.bbrc.2012.02.101 22390928

35. Wang D, Zhang Y, Zhang Z, Zhu J, Yu J. KaKs_Calculator 2.0: a toolkit incorporating gamma-series methods and sliding window strategies. Genomics Proteomics Bioinformatics. 2010; 8(1): 77–80. doi: 10.1016/S1672-0229(10)60008-3 20451164

36. Chen LY, Zhao SY, Wang QF, Moody ML. Transcriptome sequencing of three Ranunculus species (Ranunculaceae) reveals candidate genes in adaptation from terrestrial to aquatic habitats. Sci Rep. 2015; 5: 10098. doi: 10.1038/srep10098 25993393

37. Swanson WJ, Wang A, Wolfner MF, Aquadro CF. Evolutionary expressed sequence tag analysis of Drosophila female reproductive tracts identifies genes subjected to positive selection. Genetics. 2004; 168(3): 1457–1465. doi: 10.1534/genetics.104.030478 15579698

38. Chen C, Chen H, He Y, Xia R. TBtools, a toolkit for biologists integrating various biological data handling tools with a user-friendly interface. bioRxiv. 2018; p.289660.

39. Madeira F, Park Y, Lee J, Buso N, Gur T, Madhusoodanan N, et al. The EMBL-EBI search and sequence analysis tools APIs in 2019. Nucleic Acids Res. 2019; 47(W1): W636–W641. doi: 10.1093/nar/gkz268 30976793

40. Rastrick SP, Whiteley NM. Influence of natural thermal gradients on whole animal rates of protein synthesis in marine gammarid amphipods. PloS One. 2013; 8(3): e60050. doi: 10.1371/journal.pone.0060050 23544122

41. Ravaux J, Gaill F, Bris NL, Sarradin PM, Jollivet D, Shillito B. Heat-shock response and temperature resistance in the deep-sea vent shrimp Rimicaris exoculata. J Exp Biol. 2003; 206: 2345–2354. doi: 10.1242/jeb.00419 12796451

42. Hutchison JS, Moldave K. The effect of elevated temperature on protein synthesis in cell-free extracts of cultured Chinese hamster ovary cells. Biochem Biophys Res Commun. 1981; 99(2): 722–728. doi: 10.1016/0006-291x(81)91803-9 7236297

43. Hawkins AJ, Day AJ. Metabolic interrelations underlying the physiological and evolutionary advantages of genetic diversity. Integr Comp Biol. 1999; 39(2): 401–411.

44. Tang B, Wang S, Wang SG, Wang HJ, Zhang JY, Cui SY. Invertebrate trehalose-6-phosphate synthase gene: genetic architecture, biochemistry, physiological function, and potential applications. Front Physiol. 2018; 9: 30. doi: 10.3389/fphys.2018.00030 29445344

45. Virgilio CD, Hottiger T, Dominguez J, Boller T, Wiemken A. The role of trehalose synthesis for the acquisition of thermotolerance in yeast. I. Genetic evidence that trehalose is a thermoprotectant. FEBS J. 1994; 219(1–2): 179–186.

46. Paul S, Paul S. Molecular insights into the role of aqueous trehalose solution on temperature induced protein denaturation. J Phys Chem B. 2015; 119(4): 1598–1610. doi: 10.1021/jp510423n 25558880

47. Bailly X, Vinogradov S. The sulfide binding function of annelid hemoglobins: relic of an old biosystem? J Inorg Biochem. 2005; 99(1): 142–150. doi: 10.1016/j.jinorgbio.2004.10.012 15598498

48. Pradillon F, Gaill F. Adaptation to deep-sea hydrothermal vents: some molecular and developmental aspects. Journal of Marine Science and Technology. 2007; 15(15_S): 37–53.

49. Mann K, Mechling DE, Bächinger HP, Eckerskorn C, Gaill F, Timpl R. Glycosylated threonine but not 4-hydroxyproline dominates the triple helix stabilizing positions in the sequence of a hydrothermal vent worm cuticle collagen. J Mol Biol. 1996; 261(2): 255–266. doi: 10.1006/jmbi.1996.0457 8757292

50. Merzendorfer H, Zimoch L. Chitin metabolism in insects: structure, function and regulation of chitin synthases and chitinases. J Exp Biol. 2003; 206: 4393–4412. doi: 10.1242/jeb.00709 14610026

51. Dias RO, Cardoso C, Pimentel AC, Damasceno TF, Ferreira C, Terra WR. The roles of mucus‐forming mucins, peritrophins and peritrophins with mucin domains in the insect midgut. Insect Mol Biol. 2018; 27(1): 46–60. doi: 10.1111/imb.12340 28833767

52. Sánchez-Salgado JL, Pereyra MA, Agundis C, Vivanco-Rojas O, Sierra-Castillo C, Alpuche-Osorno JJ, et al. Participation of lectins in crustacean immune system. Aquac Res. 2017; 48(8): 4001–4011.

53. Chu H, Mazmanian SK. Innate immune recognition of the microbiota promotes host-microbial symbiosis. Nat Immunol. 2013; 14: 668–675. doi: 10.1038/ni.2635 23778794

54. Liu XL, Ye S, Cheng CY, Li HW, Lu B, Yang WJ, et al. Identification and characterization of a symbiotic agglutination-related C-type lectin from the hydrothermal vent shrimp Rimicaris exoculata. Fish Shellfish Immun. 2019; 92: 1–10.

55. Login FH, Balmand S, Vallier A, Vincent-Monégat C, Vigneron A, Weiss-Gayet M, et al. Antimicrobial peptides keep insect endosymbionts under control. 2011; Science. 334: 362–365. doi: 10.1126/science.1209728 22021855

56. Piquet B, Shillito B, Lallier FH, Duperron S, Andersen AC. High rates of apoptosis visualized in the symbiont-bearing gills of deep-sea Bathymodiolus mussels. Plos One. 2019; 14(2): e0211499. doi: 10.1371/journal.pone.0211499 30716127

57. Cerenius L, Söderhäll K. The prophenoloxidase-activating system in invertebrates. Immunol Rev. 2004; 198(1): 116–126.

58. Egger L, Schneider J, Rhême C, Tapernoux M, Häcki J, Borner C. Serine proteases mediate apoptosis-like cell death and phagocytosis under caspase-inhibiting conditions. Cell Death Differ. 2003; 10: 1188–1203. doi: 10.1038/sj.cdd.4401288 14502242

59. Wang X. Nutritional sources analysis and the heavy-metal enrichment of the macrofauna from deep-sea chemotrophic ecosystem. Ph.D. Thesis, Institute of Oceanology, Chinese Academy of Sciences. 2018.

60. Luther GW III, Rozan TF, Taillefert M, Nuzzio DB, Meo CD, Shank TM, et al. Chemical speciation drives hydrothermal vent ecology. Nature. 2001; 410: 813–816. doi: 10.1038/35071069 11298448

61. Yahagi T, Watanabe H, Ishibashi J, Kojima S. Genetic population structure of four hydrothermal vent shrimp species (Alvinocarididae) in the Okinawa Trough, Northwest Pacific. Mar Ecol Prog Ser. 2015; 529: 159–169.

62. Sun S, Hui M, Wang M, Sha Z. The complete mitochondrial genome of the alvinocaridid shrimp Shinkaicaris leurokolos (Decapoda, Caridea): Insight into the mitochondrial genetic basis of deep-sea hydrothermal vent adaptation in the shrimp. Comp Biochem Phys D. 2018; 25: 42–52.

63. Seebacher F, Holmes S, Roosen NJ, Nouvian M, Wilson RS, Ward AJW. Capacity for thermal acclimation differs between populations and phylogenetic lineages within a species. Func Ecol. 2012; 26: 1418–1428.

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