Skip to main content
Log in

The regulatory role of arginine kinase during larval settlement of the bryozoan Bugula neritina

  • Original paper
  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

Larval attachment and metamorphosis, also collectively known as settlement, plays an important role in the life history of marine invertebrates with biphasic life cycle. Bugula neritina can settle on any substrate without substrate selection. This complex transformation usually involves an active selection process, while the larval decision to settle is regulated by both exogenous and endogenous factors. This study focuses on the involvement of arginine kinase (AK), an important enzyme that regulates energy metabolism in marine invertebrates, during larval settlement of the bryozoan Bugula neritina. We reveal that AK was highly expressed in the swimming larvae of B. neritina, while its expression was down-regulated post-attachment. When treated with AK inhibitors, the larval settlement rate was significantly decreased. In addition, the immunostaining results indicated that AK was mainly localized to the neuro-muscular cord in swimming larvae. Overall, our results suggest the involvement of AK in regulating larval settlement of B. neritina.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Chaturvedi R, Asim M, Lewis ND, Algood HM, Cover TL, Kim PY, Wilson KT (2007) l-arginine availability regulates inducible nitric oxide synthase-dependent host defense against Helicobacter pylori. Infect Immun 75(9):4305–4315

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen X, Yao P, Chu X, Hao L, Guo X, Xu B (2015) Isolation of arginine kinase from apis Cerana cerana and its possible involvement in response to adverse stress. Cell Stress Chaperon 20(1):169–183

    Article  CAS  Google Scholar 

  • El-Gayar S, Thüring-Nahler H, Pfeilschifter J, Röllinghoff M, Bogdan C (2003) Translational control of inducible nitric oxide synthase by IL-13 and arginine availability in inflammatory macrophages. J Immunol 171(9):4561–4568

    Article  CAS  PubMed  Google Scholar 

  • Eppenberger M, Eppenberger H, Kaplan N (1967) Evolution of creatine kinase. Nature 214:239–241

    Article  CAS  PubMed  Google Scholar 

  • Fuchs J, Martindale MQ, Hejnol A (2011) Gene expression in bryozoan larvae suggest a fundamental importance of pre-patterned blastemic cells in the bryozoan life-cycle. EvoDevo 2(1):131

    Article  Google Scholar 

  • Fusetani N (2004) Biofouling and antifouling. Nat Prod Rep 21(1):94–104

    Article  CAS  PubMed  Google Scholar 

  • Gobert AP, Daulouede S, Lepoivre M, Boucher JL, Bouteille B, Buguet A, Cespuglio R, Veyret B, Vincendeau P (2000) l-Arginine availability modulates local nitric oxide production and parasite killing in experimental trypanosomiasis. Infect Immun 68(8):4653–4657

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • He L, Zhang G, Qian PY (2013) Characterization of two 20 kDa-cement protein (cp20 k) homologues in Amphibalanus amphitrite. PLoS ONE 8(5):e64130

    Article  PubMed  PubMed Central  Google Scholar 

  • Hentschel BT, Emlet RB (2000) Metamorphosis of barnacle nauplii: effects of food variability and a comparison with amphibian models. Ecology 81(12):3495–3508

    Article  Google Scholar 

  • Heyland A, Degnan S, Reitzel AM (2011) Emerging patterns in the regulation and evolution of marine invertebrate settlement and metamorphosis. In: Flatt T, Heyland A (eds) Mechanisms of life history evolution: the genetics and physiology of life history traits and trade-offs. Oxford U Press, Oxford, UK, pp 29–42

    Chapter  Google Scholar 

  • Kucharski R, Maleszka R (1998) Arginine kinase is highly expressed in the compound eye of the honey-bee, Apis mellifera. Gene 211(2):343–349

    Article  CAS  PubMed  Google Scholar 

  • Kulathunga D, Wickramasinghe S, Rajapakse R, Yatawara L, Jayaweera W, Agatsuma T (2012) Immunolocalization of arginine kinase (AK) in Toxocara canis, Toxocara vitulorum, and Ascaris lumbricoides. Parasitol Res 111(2):663–671

    Article  CAS  PubMed  Google Scholar 

  • Lang AB, Wyss C, Eppenberger HM (1980) Localization of arginine kinase in muscle fibres of Drosophila melanogaster. J Muscle Res Cell M 1(2):147–161

    Article  CAS  Google Scholar 

  • Lee J, Ryu H, Ferrante RJ, Morris SM Jr, Ratan RR (2003) Translational control of inducible nitric oxide synthase expression by arginine can explain the arginine paradox. Proc Natl Acad Sci USA 100(8):4843–4848

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Marchler-Bauer A, Derbyshire MK, Gonzales NR, Lu S, Chitsaz F, Geer LY, Geer RC, He J, Gwadz M, Hurwitz DI, Lanczycki CJ, Lu F, Marchler GH, Song JS, Thanki N, Wang Z, Yamashita AR, Zhang D, Zheng C, Bryant S (2015) CDD: NCBI’s conserved domain database. Nucleic Acids Res 43:D222–D226 (database issue)

    Article  CAS  PubMed  Google Scholar 

  • Matthews BF, Macdonald MH, Thai VK, Tucker ML (2003) Molecular characterization of arginine kinases in the soybean cyst nematode (Heterodera glycines). J Nematol 35(3):252–258

    CAS  PubMed  PubMed Central  Google Scholar 

  • Newsholme EA, Beis I, Leech AR, Zammit VA (1978) The role of creatine kinase and arginine kinase in muscle. Biochem J 172(3):533–537

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pawlik JR (1992) Chemical ecology of the settlement of benthic marine invertebrates. Oceanogr Mar Biol Annu Rev 30:273–335

    Google Scholar 

  • Pereira CA, Alonso GD, Paveto MC, Iribarren A, Cabanas ML, Torres HN, Flawiá MM (2000) Trypanosoma cruzi arginine kinase characterization and cloning a novel energetic pathway in protozoan parasites. J Biol Chem 275(2):1495–1501

    Article  CAS  PubMed  Google Scholar 

  • Qian PY, Wong YH, Zhang Y (2010) Changes in the proteome and phosphoproteome expression in the bryozoan Bugula neritina larvae in response to the antifouling agent butenolide. Proteomics 10(19):3435–3446. https://doi.org/10.1002/pmic.201000199

    Article  CAS  PubMed  Google Scholar 

  • Reed CG, Woollacott RM (1983) Mechanisms of rapid morphogenetic movements in the metamorphosis of the bryozoan Bugula neritina (cheilostomata, cellularioidea): II. The role of dynamic assemblages of microfilaments in the pallial epithelium. J Morphol 177(2):127–143

    Article  Google Scholar 

  • Santagata S (2008) Evolutionary and structural diversification of the larval nervous system among marine bryozoans. Biol Bull 215(1):3–23

    Article  PubMed  Google Scholar 

  • Shilling FM, Hoegh-Guldberg O, Manahan DT (1996) Sources of energy for increased metabolic demand during metamorphosis of the abalone Haliotis rufescens (mollusca). Biol Bull 191(3):402–412

    Article  CAS  PubMed  Google Scholar 

  • Shimizu K, Hunter E, Fusetani N (2000) Localisation of biogenic amines in larvae of Bugula neritina (Bryozoa: Cheilostomatida) and their effects on settlement. Mar Biol 136(1):1–9

    Article  CAS  Google Scholar 

  • Suzuki T, Kamidochi M, Inoue N, Kawamichi H, Yazawa Y, Furukohri T, Ellington WR (1999) Arginine kinase evolved twice: evidence that echinoderm arginine kinase originated from creatine kinase. Biochem J 340(3):671–675

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thiyagarajan V, Harder T, Qian PY (2002) Relationship between cyprid energy reserves and metamorphosis in the barnacle Balanus amphitrite darwin (cirripedia; Thoracica). J Exp Mar Biol Ecol 280(1):79–93

    Article  Google Scholar 

  • Videla J, Chaparro O, Thompson R, Concha I (1998) Role of biochemical energy reserves in the metamorphosis and early juvenile development of the oyster Ostrea chilensis. Mar Biol 132(4):635–640

    Article  Google Scholar 

  • Wang H, Zhang L, Zhang L, Lin Q, Liu N (2009) Arginine kinase: differentiation of gene expression and protein activity in the red imported fire ant, Solenopsis invicta. Gene 430(1):38–43

    Article  CAS  PubMed  Google Scholar 

  • Wang H, Zhang H, Wong YH, Voolstra C, Ravasi T, B Bajic V, Qian PY (2010) Rapid transcriptome and proteome profiling of a non-model marine invertebrate, Bugula neritina. Proteomics 10(16):2972–2981

    Article  CAS  PubMed  Google Scholar 

  • Wang K, Liu R, Li J, Mao J, Lei Y, Wu J, Zeng J, Zhang T, Wu H, Chen L, Huang C, Wei Y (2011) Quercetin induces protective autophagy in gastric cancer cells: Involvement of akt-mTOR-and hypoxia-induced factor 1α-mediated signaling. Autophagy 7(9):966–978

    Article  CAS  PubMed  Google Scholar 

  • Wendt DE (2000) Energetics of larval swimming and metamorphosis in four species of bugula (bryozoa). Biol Bull 198(3):346–356

    Article  CAS  PubMed  Google Scholar 

  • Wong YH, Wang H, Ravasi T, Qian PY (2012) Involvement of wnt signaling pathways in the metamorphosis of the bryozoan Bugula neritina. PLoS ONE 7(3):e33323

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wong YH, Ryu T, Seridi L, Ghosheh Y, Bougouffa S, Qian PY, Ravasi T (2014) Transcriptome analysis elucidates key developmental components of bryozoan lophophore development. Sci Rep UK 4:6534

    Article  CAS  Google Scholar 

  • Woollacott RM, Zimmer RL (1971) Attachment and metamorphosis of the cheiloctenostome bryozoan Bugula neritina (linné). J Morphol 134(3):351–382

    Article  Google Scholar 

  • Wu X, Zhu W, Lü Z, Xia Y, Yang J, Zou F, Wang X (2009) The effect of rutin on arginine kinase: inhibition kinetics and thermodynamics merging with docking simulation. Int J Biol Macromol 44(2):149–155

    Article  CAS  PubMed  Google Scholar 

  • Yamamoto H, Satuito CG, Yamazaki M, Natoyama K, Tachibana A, Fusetani N (1998) Neurotransmitter blockers as antifoulants against planktonic larvae of the barnacle Balanus amphitrite and the mussel Mytilus galloprovincialis. Biofouling 13(1):69–82

    Article  CAS  Google Scholar 

  • Yao C, Wu C, Xiang J, Dong B (2005) Molecular cloning and response to laminarin stimulation of arginine kinase in haemolymph in chinese shrimp, Fenneropenaeus chinensis. Fish Shellfish Immunol 19(4):317–329

    Article  CAS  PubMed  Google Scholar 

  • Zammit VA, Newsholme EA (1976) The maximum activities of hexokinase, phosphorylase, phosphofructokinase, glycerol phosphate dehydrogenases, lactate dehydrogenase, octopine dehydrogenase, phosphoenolpyruvate carboxykinase, nucleoside diphosphatekinase, glutamate-oxaloacetate transaminase and arginine kinase in relation to carbohydrate utilization in muscles from marine invertebrates. Biochem J 160(3):447–462

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang H, Wong YH, Wang H, Chen Z, Arellano SM, Ravasi T, Qian PY (2010a) Quantitative proteomics identify molecular targets that are crucial in larval settlement and metamorphosis of Bugula neritina. J Proteome Res 10(1):349–360

    Article  PubMed  Google Scholar 

  • Zhang Y, Xu Y, Arellano SM, Xiao K, Qian PY (2010b) Comparativeproteome and phosphoproteome analyses during cyprid development of the barnacle Balanus (=Amphibalanus) amphitrite. J Proteome Res 9:3146–3157

    Article  CAS  PubMed  Google Scholar 

  • Zhang G, He LS, Wong YH, Qian PY (2013) MKK3 was involved in larval settlement of the barnacle Amphibalanus amphitrite through activating the kinase activity of p38MAPK. PLoS ONE 8(7):e69510

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang Y, Sun J, Zhang H, Chandramouli KH, Xu Y, He LS, Ravasi T, Qian PY (2014) Proteomic profiling during the pre-competent to competent transition of the biofouling polychaete Hydroides elegans. Biofouling 30(8):921–928. https://doi.org/10.1080/08927014.2014.951341

    Article  CAS  PubMed  Google Scholar 

  • Zhang G, Yan G, Yang X, Wong Y, Sun J, Zhang Y, He L, Xu Y, Qian PY (2016) Characterization of arginine kinase in the barnacle Amphibalanus amphitrite and its role in the larval settlement. J Exp Zool B Mol Dev Evol 326(4):237–249

    Article  CAS  PubMed  Google Scholar 

  • Zhou G, Somasundaram T, Blanc E, Parthasarathy G, Ellington WR, Chapman MS (1998) Transition state structure of arginine kinase: implications for catalysis of bimolecular reactions. Proc Natl Acad Sci USA 95(15):8449–8454

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This work was supported by Research Grants Council of the Hong Kong Special Administrative Region (Grant nos. GRF16101015 and GRF662413) to Pei-Yuan Qian and as well as grants from Scientific and Technical Innovation Council of Shenzhen (Grant nos. 827000012, JCYJ20150625102622556, KQJSCX2017033011020642) and Guangdong Natural Science Foundation (Grant no. 2014A030310230) to Yu Zhang.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Pei-Yuan Qian.

Ethics declarations

Conflict of interest

The authors have declared no conflict of interest.

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

Additional information

Responsible Editor: F. Weinberger.

Reviewed by W. Biggers and undisclosed experts.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 144 kb)

Supplementary material 2 (DOC 33 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhang, Y., Yang, XX., Wong, YH. et al. The regulatory role of arginine kinase during larval settlement of the bryozoan Bugula neritina. Mar Biol 165, 52 (2018). https://doi.org/10.1007/s00227-018-3307-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00227-018-3307-1

Navigation