Regulatory effects of mussel (Aulacomya maoriana Iredale 1915) larval settlement by neuroactive compounds, amino acids and bacterial biofilms

Abstract

Please cite this article as: Alfaro, Andrea C., Young, Tim, Ganesan, Annapoorna Maitrayee, Regulatory effects of mussel (Aulacomya maoriana Iredale 1915) larval settlement by neuroactive compounds, amino acids and bacterial biofilms, Aquaculture (2011), doi: 10.1016/j.aquaculture.2011.08.038 This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. Pseudoalteromonas sp. AMGP1 were tested for their abilities to induce larval settlement. Toxicity effects of each treatment also were simultaneously identified by recording larval mortalities. Results indicate that all chemicals used induced larvae to settle, with acetylcholine being the most effective (~24% at 10 -6 M compared to <2% in control assays). Toxicities of treatment compounds were low at optimal settlement inducing concentrations, except for L-Tryptophan (~32%) and GABA (~59%). Our data suggest that catecholamines (and their precursors) play an important role in the biochemical mechanisms of settlement for A. maoriana. While serotonin precursors did induce low levels of larval settlement at some concentrations, high toxicity responses to 5-HTP at 10 -5 M, combined with complete settlement inhibition indicate A C C E P T E D M A N U S C R I P T ACCEPTED MANUSCRIPTthat the mechanism of action may be more complex than can be elucidated in this study. Larval settlement responses to bacterial treatments were low for planktonic and biofilm phases across all three strains, and settlement inhibition was observed when larvae were exposed to biofilm exudates of all bacterial strains. Comparisons of A. maoriana responses to other endemic and worldwide distributed mussel species are provided as a means to highlight potential evolutionary differences in chemoreception mechanisms. Highlights 1.Mussel larval settlement responses were tested with neuroactive compounds amino acids, and bacterial biofilms.2. All chemicals induced larvae to settle, with acetylcholine being the most effective.3. Catecholamines (and their precursors) play an important role in the biochemical mechanisms of settlement for A. maoriana. Settlement responses to serotonin precursors require further investigationsince there were high toxicity responses.5. Larval settlement responses to bacterial treatments were low for planktonic and biofilm phases, and exposure to biofilm exudates resulted in settlement inhibition.

Induction of settlement in larvae of the mussel Mytilus galloprovincialis using neuroactive compounds

“…GABA was also acutely toxic for P. canaliculus, with an LC50 of 1.7 * 10 − 4 M and for A. maoriana , although LC50 values were not provided for this species. Based on its highly acute toxic effect, Alfaro et al (2011) inferred that GABA would be unlikely to be a natural settlement cue, and our results reinforce this hypothesis. LC50 value for epinephrine (4.3 * 10 − 4 M) was also fairly high, however mortality was enhanced only in the higher concentration tested.…”

“…The mechanism by which GABA is able to induce settlement and metamorphosis in bivalves remains elusive. Yu et al (2008) reviewed that GABA impairs ciliar activity in mollusk larvae; Alfaro et al (2011) proposed an indirect mechanism of action by means of secretion of other substances. On the other hand, the current study reports for the first time to our knowledge the toxic effect displayed by GABA on M. galloprovincialis larvae: GABA enhanced mortality at all the concentrations tested, suggesting that this chemical would not act as a natural settlement promoter in larvae, which was also suggested byAlfaro et al (2011) for A. maoriana.…”

Neurophysiological control of swimming behaviour, attachment and metamorphosis in black-footed abalone (Haliotis iris) larvae

“…It is unclear whether this effect was caused by a coupling of the metamorphic gene regulatory network to the induced pre-metamorphic behavior/process prior to the event, or whether acetylcholine is directly involved in the morphogenic signalling pathway during the event. While acetylcholine is a potent inducer of larval settlement in some bivalve species (Yu et al 2008;Alfaro et al 2011;Young et al 2011;Sánchez-Lazo et al 2012), no effect on attachment or metamorphosis has been observed in the five Haliotis spp. tested thus far (H. discus [Fukazawa et al 2001], H. discus hannai [Akashige et al 1981], H. diversilcolor supertexta [Yu et al 2010], H. gigantea [Fukazawa et al 2001], H. rufescens [Morse et al 1979]).…”

“…It is unclear whether this effect was caused by a coupling of the metamorphic gene regulatory network to the induced pre-metamorphic behavior/process prior to the event, or whether acetylcholine is directly involved in the 17 morphogenic signalling pathway during the event. While acetylcholine is a potent inducer of larval settlement in some bivalve species (Yu et al 2008;Alfaro et al 2011;Young et al 2011;Sánchez-Lazo et al 2012) Resembling the effects of GABA, KCl, acetylcholine and dopamine, glutamine also reduced swimming activity in H. iris larvae within the first two days of exposure. Although there was some indication of induced attachment at high concentrations (10 -4 mol L -1 ), high mortalities (ca.…”

Effect of neuroactive compounds on larval metamorphosis of New Zealand geoduck (Panopea zelandica )

“…Larval settlement and metamorphosis are thought to be typically activated by various exogenous chemicals and other environmental stimuli (Hadfield & Paul ). Several physical, biological and chemical cues have been identified as inducers of larval settlement and/or metamorphosis across molluscan species (Hadfield & Paul ; Alfaro, Young, & Ganesan ). Such cues include substrate morphology (Hadfield & Paul ; Alfaro & Jeffs ), vibration (Rittschof, Forward, Cannon, Welch, McClary, Holm, Clare, Conova, McKelvey, Bryan, & van Dover ), water motion (Alfaro ), sound (Lillis, Eggleston, & Bohnenstiehl ), microbial biofilms (Ganesan, Alfaro, Brooks, & Higgins ; Tung & Alfaro ; Ganesan, Alfaro, Higgins, & Brooks ; Ganesan, Alfaro, Higgins, Duxbury, & Brooks ), the presence/absence of conspecifics and/or prey species (Hadfield & Paul ), and a range of natural or artificial chemicals (Steinberg, De Nys, & Kjelleberg ; Alfaro, Copp, Appleton, Kelly, & Jeffs ; Young, Alfaro, & Robertson ; Alfaro, Young, & Bowden ; Young, Alfaro, Sánchez‐Lazo, & Robertson ).…”