Fish & Shellfish Immunology 40 (2014) 407e413
Contents lists available at ScienceDirect
Fish & Shellfish Immunology journal homepage: www.elsevier.com/locate/fsi
Short communication
Gender-specific metabolic responses in hepatopancreas of mussel Mytilus galloprovincialis challenged by Vibrio harveyi Xiaoli Liu*, Hushan Sun, Yiyan Wang, Mengwen Ma, Yuemei Zhang School of Life Sciences, Ludong University, Yantai 264025, PR China
a r t i c l e i n f o
a b s t r a c t
Article history: Received 12 July 2014 Received in revised form 28 July 2014 Accepted 3 August 2014 Available online 11 August 2014
Mussel Mytilus galloprovincialis is a marine aquaculture shellfish and frequently studied in shellfish immunology. In this work, the gender-specific metabolic responses induced by Vibrio harveyi in hepatopancreas from M. galloprovincialis were characterized using NMR-based metabolomics. In details, V. harveyi challenge increased the levels of amino acids including (valine, leucine, isoleucine, threonine, alanine, arginine and tyrosine) and ATP, and decreased the level of glucose in male mussel hepatopancreas. In V. harveyi-challenged female mussel hepatopancreas, both threonine and AMP were significantly elevated, and choline, phoshphocholine, sn-glycero-3-phosphocholine, taurine, betaine and ATP were depleted. Obviously, only threonine was similarly altered to that in V. harveyi-challenged male mussel hepatopancreas. These findings confirmed the gender-specific metabolic responses in mussels challenged by V. harveyi. Overall, V. harveyi induced an enhanced energy demand through activated glycolysis and immune response indicated by increased BCAAs in male mussel hepatopancreas. In female mussel hepatopancreas, V. harveyi basically caused disturbances in both osmotic regulation and energy metabolism through the metabolic pathways of conversions of phosphocholine and ADP to choline and ATP, and sn-glycero-3-phosphocholine and H2O into choline and sn-glycerol 3-phosphate. The altered mRNA expression levels of related genes (Cu/Zn-SOD, HSP90, lysozyme and defensin) suggested that V. harveyi induced obvious oxidative and immune stresses in both male and female mussel hepatopancreas. This work demonstrated that V. harveyi could induce gender-specific metabolic responses in mussel M. galloprovincialis hepatopancreas using NMR-based metabolomics. © 2014 Elsevier Ltd. All rights reserved.
Keywords: Mytilus galloprovincialis Hepatopancreas Gender-specific responses Vibrio harveyi Metabolomics
1. Introduction The outbreak of vibrios, such as Vibrio anguillarum, Vibrio alginolyticus, Vibrio splendidus, Vibrio furnissii, Vibrio parahaemolyticus, Vibrio tapetis and Vibrio harveyi, can induce severe vibriosis in both fish and shellfish [1,2]. Among these vibrios, V. harveyi is an important causative pathogen for the massive mortality of marine aquaculture animals including fish, crustacean and bivalves in marine environments [3,4]. Recent immunity studies have indicated that vibrio pathogens can induce oxidative stress, immune stress, DNA damage, protein denaturation and disruption in energy metabolism, in mollusks, such as mussel Mytilus galloprovincialis and scallop Chlamys farreri [5e7]. Marine mussel M. galloprovincialis distributes widely along the coast in north China and can be consumed as delicious seafood by local residents. As a filter-
* Corresponding author. Tel.: þ86 535 6696155; fax: þ86 535 6696598. E-mail address: [email protected] (X. Liu). http://dx.doi.org/10.1016/j.fsi.2014.08.002 1050-4648/© 2014 Elsevier Ltd. All rights reserved.
feeder, M. galloprovincialis is often used as a preferable bioindicator in marine ecotoxicology and biomonitoring programs due to its high accumulation of environmental contaminants [8,9]. Moreover, M. galloprovincialis is also frequently used in shellfish immunology studies because of its high susceptibility to pathogens [10e12]. Canesi et al. reported that both V. splendidus and V. anguillarum challenges caused obvious oxidative and immune stresses in mussel M. galloprovincialis, marked by the significant over-expression levels of catalase, glutathione transferase, lysozymes and metallothioneins that are involved in anti-oxidant and immune systems [11]. In spite of many shellfish immunology studies, the biochemical mechanisms of pathogen-induced effects in M. galloprovincialis were partly elucidated by the special immune-stress responsive molecules [10e13], the global responsive mechanisms have not fully characterized. One way to obtain a global view of responsive mechanisms of organisms to stressors is to apply the eomics techniques, such as genomics, transcriptomics, proteomics and metabolomics [5,14e18]. Among these eomics techniques,
408
X. Liu et al. / Fish & Shellfish Immunology 40 (2014) 407e413
metabolomics focuses on the whole set of metabolites with small molecular weight (
Contents lists available at ScienceDirect
Fish & Shellfish Immunology journal homepage: www.elsevier.com/locate/fsi
Short communication
Gender-specific metabolic responses in hepatopancreas of mussel Mytilus galloprovincialis challenged by Vibrio harveyi Xiaoli Liu*, Hushan Sun, Yiyan Wang, Mengwen Ma, Yuemei Zhang School of Life Sciences, Ludong University, Yantai 264025, PR China
a r t i c l e i n f o
a b s t r a c t
Article history: Received 12 July 2014 Received in revised form 28 July 2014 Accepted 3 August 2014 Available online 11 August 2014
Mussel Mytilus galloprovincialis is a marine aquaculture shellfish and frequently studied in shellfish immunology. In this work, the gender-specific metabolic responses induced by Vibrio harveyi in hepatopancreas from M. galloprovincialis were characterized using NMR-based metabolomics. In details, V. harveyi challenge increased the levels of amino acids including (valine, leucine, isoleucine, threonine, alanine, arginine and tyrosine) and ATP, and decreased the level of glucose in male mussel hepatopancreas. In V. harveyi-challenged female mussel hepatopancreas, both threonine and AMP were significantly elevated, and choline, phoshphocholine, sn-glycero-3-phosphocholine, taurine, betaine and ATP were depleted. Obviously, only threonine was similarly altered to that in V. harveyi-challenged male mussel hepatopancreas. These findings confirmed the gender-specific metabolic responses in mussels challenged by V. harveyi. Overall, V. harveyi induced an enhanced energy demand through activated glycolysis and immune response indicated by increased BCAAs in male mussel hepatopancreas. In female mussel hepatopancreas, V. harveyi basically caused disturbances in both osmotic regulation and energy metabolism through the metabolic pathways of conversions of phosphocholine and ADP to choline and ATP, and sn-glycero-3-phosphocholine and H2O into choline and sn-glycerol 3-phosphate. The altered mRNA expression levels of related genes (Cu/Zn-SOD, HSP90, lysozyme and defensin) suggested that V. harveyi induced obvious oxidative and immune stresses in both male and female mussel hepatopancreas. This work demonstrated that V. harveyi could induce gender-specific metabolic responses in mussel M. galloprovincialis hepatopancreas using NMR-based metabolomics. © 2014 Elsevier Ltd. All rights reserved.
Keywords: Mytilus galloprovincialis Hepatopancreas Gender-specific responses Vibrio harveyi Metabolomics
1. Introduction The outbreak of vibrios, such as Vibrio anguillarum, Vibrio alginolyticus, Vibrio splendidus, Vibrio furnissii, Vibrio parahaemolyticus, Vibrio tapetis and Vibrio harveyi, can induce severe vibriosis in both fish and shellfish [1,2]. Among these vibrios, V. harveyi is an important causative pathogen for the massive mortality of marine aquaculture animals including fish, crustacean and bivalves in marine environments [3,4]. Recent immunity studies have indicated that vibrio pathogens can induce oxidative stress, immune stress, DNA damage, protein denaturation and disruption in energy metabolism, in mollusks, such as mussel Mytilus galloprovincialis and scallop Chlamys farreri [5e7]. Marine mussel M. galloprovincialis distributes widely along the coast in north China and can be consumed as delicious seafood by local residents. As a filter-
* Corresponding author. Tel.: þ86 535 6696155; fax: þ86 535 6696598. E-mail address: [email protected] (X. Liu). http://dx.doi.org/10.1016/j.fsi.2014.08.002 1050-4648/© 2014 Elsevier Ltd. All rights reserved.
feeder, M. galloprovincialis is often used as a preferable bioindicator in marine ecotoxicology and biomonitoring programs due to its high accumulation of environmental contaminants [8,9]. Moreover, M. galloprovincialis is also frequently used in shellfish immunology studies because of its high susceptibility to pathogens [10e12]. Canesi et al. reported that both V. splendidus and V. anguillarum challenges caused obvious oxidative and immune stresses in mussel M. galloprovincialis, marked by the significant over-expression levels of catalase, glutathione transferase, lysozymes and metallothioneins that are involved in anti-oxidant and immune systems [11]. In spite of many shellfish immunology studies, the biochemical mechanisms of pathogen-induced effects in M. galloprovincialis were partly elucidated by the special immune-stress responsive molecules [10e13], the global responsive mechanisms have not fully characterized. One way to obtain a global view of responsive mechanisms of organisms to stressors is to apply the eomics techniques, such as genomics, transcriptomics, proteomics and metabolomics [5,14e18]. Among these eomics techniques,
408
X. Liu et al. / Fish & Shellfish Immunology 40 (2014) 407e413
metabolomics focuses on the whole set of metabolites with small molecular weight (
