Transcriptome analysis provides insights into a molecular mechanism of histamine response in the cyprid larvae of Amphibalanus amphitrite

: Barnacles are notorious marine fouling creatures; their planktonic cyprid larvae attach to material substrates and metamorphose. Histamine has shown great importance in regulating cyprid settlement and metamorphosis. This study aimed to investigate the mechanisms of histamine-induced larval settlement. Cyprids were exposed to histamine or loratadine, an anti-histamine compound. The percent larval settlements of the histamine-and anti-histamine-treated cyprids were significantly higher and lower, respectively, than the control group. Transcriptomic analyses showed that histamine-treated cyprids had 18 498 differentially expressed genes (DEGs, 14 531 up-regulated, 3967 down-regulated) and the anti-histamine group had 18 055 DEGs (17 237 up-regulated, 818 down-regulated) in comparison to untreated controls. In both treatment groups, significant enrichment of DEGs involved in the mitogen-activated protein kinase signaling pathway was observed. Based on the results of larval settlement bioassays, we set 4 filter conditions to perform DEG analyses, and 19 DEGs were selected as functional genes related to cyprid settlement. The functional categories of these genes included structural proteins, spider silk proteins, energy metabolism proteins, cement proteins, glycosyl proteins, and multifunctional proteins. The energy metabolism protein AdipoR was significantly up-regulated in the histamine-treated cyprids but significantly down-regulated in the anti-histamine group. The activity of adenosine monophosphate-activated protein kinase, a downstream signaling protein of AdipoR, increased in the histamine-treated group and decreased in the anti-histamine-treated group. Our results provide new insights into the molecular mechanisms underlying the histamine-induced settlement of barnacle cyprids and identify AdipoR as an im portant gene that can affect the settlement of cyprids, likely through regulating cyprid energy metabolism.

[1]  Liying Chen,et al.  Adenosine Triggers Larval Settlement and Metamorphosis in the Mussel Mytilopsis sallei through the ADK-AMPK-FoxO Pathway. , 2021, ACS chemical biology.

[2]  T. Simas,et al.  Marine Biofouling: A European Database for the Marine Renewable Energy Sector , 2020, Journal of Marine Science and Engineering.

[3]  Fuhua Li,et al.  Comparative transcriptomic analysis of deep- and shallow-water barnacle species (Cirripedia, Poecilasmatidae) provides insights into deep-sea adaptation of sessile crustaceans , 2020, BMC Genomics.

[4]  S. Dobretsov,et al.  Love at First Taste: Induction of Larval Settlement by Marine Microbes , 2020, International journal of molecular sciences.

[5]  S. G. Dedos,et al.  Should I stay or should I go? The settlement-inducing protein complex guides barnacle settlement decisions , 2018, Journal of Experimental Biology.

[6]  Yu Zhang,et al.  Exploring the regulatory role of nitric oxide (NO) and the NO-p38MAPK/cGMP pathway in larval settlement of the bryozoan Bugula neritina , 2018, Biofouling.

[7]  Thomas Shafee,et al.  Transcriptomics technologies , 2017, PLoS Comput. Biol..

[8]  C. Spillmann,et al.  Barnacle biology before, during and after settlement and metamorphosis: a study of the interface , 2017, Journal of Experimental Biology.

[9]  Christopher R. So,et al.  Sequence basis of Barnacle Cement Nanostructure is Defined by Proteins with Silk Homology , 2016, Scientific Reports.

[10]  Hyun-Woo Kim,et al.  Molecular characterization of an adiponectin receptor homolog in the white leg shrimp, Litopenaeus vannamei , 2016, PeerJ.

[11]  I. Tabarean.  Histamine receptor signaling in energy homeostasis , 2016, Neuropharmacology.

[12]  J. Sun,et al.  Characterization of Arginine Kinase in the Barnacle Amphibalanus Amphitrite and Its Role in the Larval Settlement. , 2016, Journal of experimental zoology. Part B, Molecular and developmental evolution.

[13]  S. Bougouffa,et al.  Transcriptome analysis elucidates key developmental components of bryozoan lophophore development , 2014, Scientific Reports.

[14]  Li Miao,et al.  Histamine promotes the larval metamorphic competence of barnacle Amphibalanus amphitrite , 2014 .

[15]  Li Miao,et al.  Antifouling activities of anti-histamine compounds against the barnacle Amphibalanus (= Balanus) amphitrite , 2014 .

[16]  Hsiu-Chin Lin,et al.  First study on gene expression of cement proteins and potential adhesion-related genes of a membranous-based barnacle as revealed from Next-Generation Sequencing technology , 2014, Biofouling.

[17]  Yu Zhang,et al.  Evidence for the Involvement of p38 MAPK Activation in Barnacle Larval Settlement , 2012, PloS one.

[18]  Jin Sun,et al.  Transcriptomic Analysis of Neuropeptides and Peptide Hormones in the Barnacle Balanus amphitrite: Evidence of Roles in Larval Settlement , 2012, PloS one.

[19]  A. Clare,et al.  Metamorphosis in the Cirripede Crustacean Balanus amphitrite , 2012, PloS one.

[20]  Mukesh Jain.  Next-generation sequencing technologies for gene expression profiling in plants. , 2012, Briefings in functional genomics.

[21]  Colin N. Dewey,et al.  RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome , 2011, BMC Bioinformatics.

[22]  V. Bajic,et al.  Toward an Understanding of the Molecular Mechanisms of Barnacle Larval Settlement: A Comparative Transcriptomic Approach , 2011, PloS one.

[23]  N. Friedman,et al.  Trinity: reconstructing a full-length transcriptome without a genome from RNA-Seq data , 2011, Nature Biotechnology.

[24]  Yukita Sato,et al.  Regulation of synthesis and oxidation of fatty acids by adiponectin receptors (AdipoR1/R2) and insulin receptor substrate isoforms (IRS-1/-2) of the liver in a nonalcoholic steatohepatitis animal model. , 2011, Metabolism: clinical and experimental.

[25]  M. Schultz,et al.  Economic impact of biofouling on a naval surface ship , 2011, Biofouling.

[26]  Hao Wang,et al.  Involvement of a novel p38 mitogen-activated protein kinase in larval metamorphosis of the polychaete Hydroides elegans (Haswell). , 2010, Journal of experimental zoology. Part B, Molecular and developmental evolution.

[27]  Y. Hayashi,et al.  Adiponectin and AdipoR1 regulate PGC-1α and mitochondria by Ca2+ and AMPK/SIRT1 , 2010, Nature.

[28]  Matthew D. Young,et al.  Gene ontology analysis for RNA-seq: accounting for selection bias , 2010, Genome Biology.

[29]  A. C. Anil,et al.  What do barnacle larvae feed on? Implications in biofouling ecology , 2009, Journal of the Marine Biological Association of the United Kingdom.

[30]  M. Hay.  Marine chemical ecology: chemical signals and cues structure marine populations, communities, and ecosystems. , 2009, Annual review of marine science.

[31]  T. Bekel,et al.  Construction of an adult barnacle (Balanus amphitrite) cDNA library and selection of reference genes for quantitative RT-PCR studies , 2009, BMC Molecular Biology.

[32]  Tao Cai,et al.  Automated genome annotation and pathway identification using the KEGG Orthology (KO) as a controlled vocabulary , 2005, Bioinform..

[33]  David Carling,et al.  The AMP-activated protein kinase cascade--a unifying system for energy control. , 2004, Trends in biochemical sciences.

[34]  John D. Storey,et al.  Statistical significance for genomewide studies , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[35]  P. Qian,et al.  Relationship between cyprid energy reserves and metamorphosis in the barnacle Balanus amphitrite Darwin (Cirripedia; Thoracica) , 2002 .

[36]  Huitu Liu,et al.  MAPK signal pathways in the regulation of cell proliferation in mammalian cells , 2002, Cell Research.

[37]  A. E. Stuart,et al.  Uptake of the Neurotransmitter Histamine into the Eyes of Larvae of the Barnacle (Balanus amphitrite) , 2002, The Biological Bulletin.

[38]  Jongkyeong Chung,et al.  Akt: versatile mediator of cell survival and beyond. , 2002, Journal of biochemistry and molecular biology.

[39]  J. Roughgarden,et al.  A LATITUDINAL GRADIENT IN RECRUITMENT OF INTERTIDAL INVERTEBRATES IN THE NORTHEAST PACIFIC OCEAN , 2001 .

[40]  M. Cobb,et al.  Mitogen-activated protein (MAP) kinase pathways: regulation and physiological functions. , 2001, Endocrine reviews.

[41]  Kiyotaka Matsumura,et al.  Nature and perception of barnacle settlement pheromones , 2000, Biofouling.

[42]  A. E. Stuart,et al.  From Fruit Flies to Barnacles, Histamine Is the Neurotransmitter of Arthropod Photoreceptors , 1999, Neuron.

[43]  N. Fusetani,et al.  Neurotransmitter blockers as antifoulants against planktonic larvae of the barnacle Balanus amphitrite and the mussel Mytilus galloprovincialis , 1998 .

[44]  N. Fusetani,et al.  Purification of a larval settlement-inducing protein complex (SIPC) of the barnacle, Balanus amphitrite , 1998 .

[45]  Jeremiah N. Jarrett.  Temporal variation in substratum specificity of Semibalanus balanoides (Linnaeus) cyprids , 1997 .

[46]  N. Fusetani,et al.  Serotonin involvement in larval settlement of the barnacle, Balanus amphitrite , 1996 .

[47]  A. Clare,et al.  Signal transduction in barnacle settlement: Calcium re-visited. , 1996, Biofouling.

[48]  D. J. Gerhart,et al.  Barnacle in vitro assays for biologically active substances: Toxicity and Settlement inhibition assays using mass cultured Balanus amphitrite amphitrite darwin , 1992 .

[49]  D. J. Gerhart,et al.  Rapid field assessment of antifouling and foul‐release coatings , 1992 .

[50]  K. Tegtmeyer,et al.  Synthetic peptide analogs to barnacle settlement pheromone , 1988, Peptides.

[51]  D. Crisp.  Recruitment of barnacle larvae from the plankton , 1985 .

[52]  D. Rittschof,et al.  Settlement and behavior in relation to flow and surface in larval barnacles, Balanus amphitrite Darwin , 1984 .

[53]  M. Lucas,et al.  An energy budget for the free-swimming and metamorphosing larvae of Balanus balanoides (Crustacea: Cirripedia) , 1979 .

[54]  D. Crisp,et al.  A field study of settlement behaviour in Balanus balanoides and Elminius modestus (Cirripedia: Crustacea) in relation to competition between them , 1979, Journal of the Marine Biological Association of the United Kingdom.

[55]  D. Crisp.  Mobility of Barnacles , 1960, Nature.