Quantitative Comparison of Caste Differences in Honeybee Hemolymph

The honeybee, Apis mellifera, is an invaluable partner in agriculture around the world both for its production of honey and, more importantly, for its role in pollination. Honeybees are largely unexplored at the molecular level despite a long and distinguished career as a model organism for understanding social behavior. Like other eusocial insects, honeybees can be divided into several castes: the queen (fertile female), workers (sterile females), and drones (males). Each caste has different energetic and metabolic requirements, and each differs in its susceptibility to pathogens, many of which have evolved to take advantage of the close social network inside a colony. Hemolymph, arthropods’ equivalent to blood, distributes nutrients throughout the bee, and the immune components contained within it form one of the primary lines of defense against invading microorganisms. In this study we have applied qualitative and quantitative proteomics to gain a better understanding of honeybee hemolymph and how it varies among the castes and during development. We found large differences in hemolymph protein composition, especially between larval and adult stage bees and between male and female castes but even between adult workers and queens. We also provide experimental evidence for the expression of several unannotated honeybee genes and for the detection of biomarkers of a viral infection. Our data provide an initial molecular picture of honeybee hemolymph, to a greater depth than previous studies in other insects, and will pave the way for future biochemical studies of innate immunity in this animal. The honeybee, Apis mellifera, is an invaluable partner in agriculture around the world both for its production of honey and, more importantly, for its role in pollination. Honeybees are largely unexplored at the molecular level despite a long and distinguished career as a model organism for understanding social behavior. Like other eusocial insects, honeybees can be divided into several castes: the queen (fertile female), workers (sterile females), and drones (males). Each caste has different energetic and metabolic requirements, and each differs in its susceptibility to pathogens, many of which have evolved to take advantage of the close social network inside a colony. Hemolymph, arthropods’ equivalent to blood, distributes nutrients throughout the bee, and the immune components contained within it form one of the primary lines of defense against invading microorganisms. In this study we have applied qualitative and quantitative proteomics to gain a better understanding of honeybee hemolymph and how it varies among the castes and during development. We found large differences in hemolymph protein composition, especially between larval and adult stage bees and between male and female castes but even between adult workers and queens. We also provide experimental evidence for the expression of several unannotated honeybee genes and for the detection of biomarkers of a viral infection. Our data provide an initial molecular picture of honeybee hemolymph, to a greater depth than previous studies in other insects, and will pave the way for future biochemical studies of innate immunity in this animal. In higher organisms, blood is responsible for supplying nutrients to tissues and organs. This fluid is a complex mixture of whole cells, proteins, lipids, carbohydrates, nucleic acids, and hormones as well as degradation products of all of these. Strictly speaking, blood is a term specific for animals with a closed circulatory system, so in arthropods, which have an open circulation, the analogous fluid is known as hemolymph. Key proteins in all adult hemolymph include transferrin (1Kucharski R. Maleszka R. Transcriptional profiling reveals multifunctional roles for transferrin in the honeybee, Apis mellifera.J. Insect. Sci. 2003; 3: 1-8Crossref PubMed Scopus (74) Google Scholar), an iron transporter; apolipophorin (2Robbs S.L. Ryan R.O. Schmidt J.O. Keim P.S. Law J.H. Lipophorin of the larval honeybee, Apis mellifera L.J. Lipid Res. 1985; 26: 241-247Abstract Full Text PDF PubMed Google Scholar, 3Shipman B.A. Ryan R.O. Schmidt J.O. Law J.H. Purification and properties of a very high density lipoprotein from the hemolymph of the honeybee Apis mellifera.Biochemistry. 1987; 26: 1885-1889Crossref PubMed Scopus (37) Google Scholar), a lipid transporter; and vitellogenin, a major nutrient storage protein in females thought to serve as a nutrient reserve and lipid carrier (4Wheeler D.E. Kawooya J.K. Purification and characterization of honey bee vitellogenin.Arch. Insect Biochem. Physiol. 1990; 14: 253-267Crossref PubMed Scopus (81) Google Scholar, 5Barchuk A.R. Bitondi M.M. Simoes Z.L. of and the of in hemolymph of queen and of Apis mellifera.J. Insect. Sci. 1-8Crossref PubMed Scopus Google The fluid also components of the innate immune system, as Insect and role in Biochem. PubMed Scopus Google Scholar), The immune of 2003; PubMed Scopus Google Scholar), and for the of Bitondi M.M. Simoes Z.L. characterization of a and its expression in Apis Biochem. PubMed Scopus Google innate immune of many to innate immunity in the study of hemolymph has largely to the and into the for biomarkers in In the a of studies have to hemolymph and proteins in is the among as have to the hemolymph of in of larval hemolymph Res. 2003; PubMed Scopus Google Scholar, of the larval hemolymph Full Text Full Text PDF PubMed Scopus Google Scholar, R. larval hemolymph protein Res. 2003; PubMed Scopus Google as well as for the of and immune proteins in Sci. 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PubMed Scopus Google Scholar, expression in the in honey 2003; PubMed Scopus Google are the to the expression of proteins in mellifera but have applied to whole and to honeybee and is of of of this of and R. R. PubMed Scopus Google and of bee The protein of honeybee a PubMed Scopus Google have in and protein of honeybee hemolymph the has and the of to protein but is very the protein of this The of this study to of honeybee hemolymph proteins the very are known as a to future biochemical studies of innate immunity in we and protein differences in this an initial molecular understanding of the susceptibility of specific castes to major honeybee and are the model for social but and to a have the of for molecular The of genes in mellifera are of the products have The data provide experimental for a large of proteins and to other of open to be are a of honeybee proteins with of expression during in different and the proteomics data previous a largely of Sci. 2003; PubMed Scopus Google Scholar), as an protein in adult and workers and (4Wheeler D.E. Kawooya J.K. Purification and characterization of honey bee vitellogenin.Arch. Insect Biochem. Physiol. 1990; 14: 253-267Crossref PubMed Scopus (81) Google Scholar, 5Barchuk A.R. Bitondi M.M. Simoes Z.L. of and the of in hemolymph of queen and of Apis mellifera.J. Insect. Sci. 1-8Crossref PubMed Scopus Google but also in drones of and of in adult honey bees Insect Physiol. Scopus Google Scholar, Simoes Z.L. expression in queen and in of both of Apis Insect Biochem. Physiol. PubMed Scopus Google of in to the adult female castes with previous of its expression Simoes Z.L. expression in queen and in of both of Apis Insect Biochem. Physiol. PubMed Scopus Google the other are a of nutrient storage proteins the of larval hemolymph The and of storage PubMed Scopus Google Scholar, and of in and hemolymph of the honeybee, Apis Biochem. PubMed Scopus Google Scholar), and the queen the caste to expression during in to also previous studies and of in and hemolymph of the honeybee, Apis Biochem. 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PubMed Scopus Google and in in to and several proteins of hemolymph proteins in to immune and PubMed Scopus Google the honeybee has an of data to in other model will for to the protein of hemolymph are one of the of and largely unexplored quantitative of different castes and data several and to at a molecular The study an of the of honeybee hemolymph will open for biochemical of this In higher organisms, blood is responsible for supplying nutrients to tissues and organs. This fluid is a complex mixture of whole cells, proteins, lipids, carbohydrates, nucleic acids, and hormones as well as degradation products of all of these. Strictly speaking, blood is a term specific for animals with a closed circulatory system, so in arthropods, which have an open circulation, the analogous fluid is known as hemolymph. Key proteins in all adult hemolymph include transferrin (1Kucharski R. Maleszka R. Transcriptional profiling reveals multifunctional roles for transferrin in the honeybee, Apis mellifera.J. Insect. Sci. 2003; 3: 1-8Crossref PubMed Scopus (74) Google Scholar), an iron transporter; apolipophorin (2Robbs S.L. Ryan R.O. Schmidt J.O. Keim P.S. Law J.H. Lipophorin of the larval honeybee, Apis mellifera L.J. Lipid Res. 1985; 26: 241-247Abstract Full Text PDF PubMed Google Scholar, 3Shipman B.A. Ryan R.O. Schmidt J.O. Law J.H. Purification and properties of a very high density lipoprotein from the hemolymph of the honeybee Apis mellifera.Biochemistry. 1987; 26: 1885-1889Crossref PubMed Scopus (37) Google Scholar), a lipid transporter; and vitellogenin, a major nutrient storage protein in females thought to serve as a nutrient reserve and lipid carrier (4Wheeler D.E. Kawooya J.K. Purification and characterization of honey bee vitellogenin.Arch. Insect Biochem. Physiol. 1990; 14: 253-267Crossref PubMed Scopus (81) Google Scholar, 5Barchuk A.R. Bitondi M.M. Simoes Z.L. of and the of in hemolymph of queen and of Apis mellifera.J. Insect. Sci. 1-8Crossref PubMed Scopus Google The fluid also components of the innate immune system, as Insect and role in Biochem. PubMed Scopus Google Scholar), The immune of 2003; PubMed Scopus Google Scholar), and for the of Bitondi M.M. Simoes Z.L. characterization of a and its expression in Apis Biochem. PubMed Scopus Google The innate immune of many to innate immunity in the study of hemolymph has largely to the and into the for biomarkers in In the a of studies have to hemolymph and proteins in is the among as have to the hemolymph of in of larval hemolymph Res. 2003; PubMed Scopus Google Scholar, of the larval hemolymph Full Text Full Text PDF PubMed Scopus Google Scholar, R. larval hemolymph protein Res. 2003; PubMed Scopus Google as well as for the of and immune proteins in Sci. PubMed Scopus Google and and of the immune of PubMed Scopus Google Scholar, proteomics for Sci. PubMed Scopus Google Scholar, The immune is Res. PubMed Scopus Google Scholar, R. R. of Res. PubMed Scopus Google hemolymph studies have also for as as of proteins during larval of Res. PubMed Scopus Google Scholar), studies of in the Biochem. PubMed Scopus Google Scholar), R. from of the female PubMed Google Scholar), and The hemolymph of Biochem. PubMed Scopus Google Scholar, of hemolymph proteins in to immune and PubMed Scopus Google its Apis mellifera has the of of even more than the study from the of honeybees for the is The of honey bees as of in and of honey is a more than and is the of of the social of honeybees has well is known the of a R. Maleszka R. and of expression in the honeybee PubMed Scopus (37) Google Scholar, D.E. during honeybee caste Scholar, and for studies of and in the honey Res. PubMed Scopus Google Scholar, expression in the in honey 2003; PubMed Scopus Google are the to the expression of proteins in mellifera but have applied to whole and to hemolymph. The honeybee and is of of of this of and R. R. PubMed Scopus Google and of bee The protein of honeybee a PubMed Scopus Google have in and protein of honeybee hemolymph the has and the of to protein but is very the protein of this The of this study to of honeybee hemolymph proteins the very are known as a to future biochemical studies of innate immunity in we and protein differences in this an initial molecular understanding of the susceptibility of specific castes to major honeybee and are the model for social but and to a have the of for molecular The of genes in mellifera are of the products have The data provide experimental for a large of proteins and to other of open to be are a of honeybee proteins with of expression during in different and the proteomics data previous a largely of Sci. 2003; PubMed Scopus Google Scholar), as an protein in adult and workers and (4Wheeler D.E. Kawooya J.K. Purification and characterization of honey bee vitellogenin.Arch. Insect Biochem. Physiol. 1990; 14: 253-267Crossref PubMed Scopus (81) Google Scholar, 5Barchuk A.R. Bitondi M.M. Simoes Z.L. of and the of in hemolymph of queen and of Apis mellifera.J. Insect. Sci. 1-8Crossref PubMed Scopus Google but also in drones of and of in adult honey bees Insect Physiol. Scopus Google Scholar, Simoes Z.L. expression in queen and in of both of Apis Insect Biochem. Physiol. PubMed Scopus Google of in to the adult female castes with previous of its expression Simoes Z.L. expression in queen and in of both of Apis Insect Biochem. Physiol. PubMed Scopus Google the other are a of nutrient storage proteins the of larval hemolymph The and of storage PubMed Scopus Google Scholar, and of in and hemolymph of the honeybee, Apis Biochem. PubMed Scopus Google Scholar), and the queen the caste to expression during in to also previous studies and of in and hemolymph of the honeybee, Apis Biochem. PubMed Scopus Google to in all high of vitellogenin, and in females is a to of proteins, analogous to the in proteomics D.E. of from PubMed Scopus Google In of the protein in of hemolymph from females a the of females the male is females a greater of proteins with the protein in females with the is the of of and to a the of a proteins the of protein proteins in in this which is one of the to for more is to proteomics for this with hemolymph proteins have from in of larval hemolymph Res. 2003; PubMed Scopus Google Scholar, of the larval hemolymph Full Text Full Text PDF PubMed Scopus Google Scholar, R. larval hemolymph protein Res. 2003; PubMed Scopus Google term of to mellifera hemolymph proteins for which are a studies for the major protein with is a of a protein found in fluid and of Full Text Full Text PDF PubMed Scopus Google and the from male of an and of the PubMed Scopus Google Scholar), an in the of to hemolymph to include proteins to are in other caste protein to be in and adult queen and hemolymph contained a protein with a role in hemolymph contained more in than adult for the of and and a better of is the of an in hemolymph. of of be throughout all of so proteins in adult bees as well but at is with which in the of the so this at a of protein for of protein in proteomics the of Full Text Full Text PDF PubMed Scopus Google long as of different is is a for the of proteins in different especially it is to all to the complex data the other protein for a protein found between high of a the and to the for a in a even it is The of this the for a in different will be and so the we proteins for this at in each all other proteins this in have to major as a for and PubMed Scopus Google so we at the with which we to a in one hemolymph and so the bees in the can but the in the to this This hemolymph be a fluid for the of other honeybee with as In are and is for to for even large but be in large as of initial of this study to the molecular components of the honeybee immune system, which is to be to both are the honeybee hemolymph found to at proteins of the and which in to and is a of the against and Simoes Z.L. Bitondi M.M. in Apis mellifera honey bee and expression of the Biochem. PubMed Scopus Google Scholar), a defense to and of in be the of its immune and be at responsible for the of in all larval of the a protein a J.H. a for and the for the of innate immune genes in Full Text Full Text PDF PubMed Scopus Google Scholar, of the 2003; PubMed Scopus Google responsible for the of and R. The in The Scholar), also found in mellifera proteins and found to be to the protein its to the of is for is a PubMed Scopus Google protein be but the protein at all in hemolymph. an and characterization of an is in the honeybee Full Text PDF PubMed Google Scholar), is in in with the protein in to expression of a protein in and of Sci. PubMed Scopus Google and to role of a protein in in of the Full Text Full Text PDF PubMed Scopus Google Scholar), which is a known of the proteins and PubMed Scopus Google The honeybee is a large protein but it is very This other of the protein in the hemolymph but are to In it is adult workers have more proteins with this is the stage and it a for the of to as and proteomics be to hemolymph from studies have in a of and other as and and of the immune of PubMed Scopus Google Scholar, proteomics for Sci. PubMed Scopus Google Scholar, The immune is Res. PubMed Scopus Google Scholar, R. R. of Res. PubMed Scopus Google in studies of in the Biochem. PubMed Scopus Google and in in to and several proteins of hemolymph proteins in to immune and PubMed Scopus Google the honeybee has an of data to in other model will for to the protein of hemolymph are one of the of and largely unexplored quantitative of different castes and data several and to at a molecular The study an of the of honeybee hemolymph will open for biochemical of this Honeybees and are the model for social but and to a have the of for molecular The of genes in mellifera are of the products have The data provide experimental for a large of proteins and to other of open to be are a of honeybee proteins with of expression during in different and the proteomics data previous a largely of Sci. 2003; PubMed Scopus Google Scholar), as an protein in adult and workers and (4Wheeler D.E. Kawooya J.K. Purification and characterization of honey bee vitellogenin.Arch. Insect Biochem. Physiol. 1990; 14: 253-267Crossref PubMed Scopus (81) Google Scholar, 5Barchuk A.R. Bitondi M.M. Simoes Z.L. of and the of in hemolymph of queen and of Apis mellifera.J. Insect. Sci. 1-8Crossref PubMed Scopus Google but also in drones of and of in adult honey bees Insect Physiol. Scopus Google Scholar, Simoes Z.L. expression in queen and in of both of Apis Insect Biochem. Physiol. PubMed Scopus Google of in to the adult female castes with previous of its expression Simoes Z.L. expression in queen and in of both of Apis Insect Biochem. Physiol. PubMed Scopus Google the other are a of nutrient storage proteins the of larval hemolymph The and of storage PubMed Scopus Google Scholar, and of in and hemolymph of the honeybee, Apis Biochem. PubMed Scopus Google Scholar), and the queen the caste to expression during in to also previous studies and of in and hemolymph of the honeybee, Apis Biochem. PubMed Scopus Google to in all The high of vitellogenin, and in females is a to of proteins, analogous to the in proteomics D.E. of from PubMed Scopus Google In of the protein in of hemolymph from females a the of females the male is females a greater of proteins with the protein in females with the is the of of and to a the of a proteins the of protein proteins in in this which is one of the to for more is to proteomics for this with hemolymph proteins have from in of larval hemolymph Res. 2003; PubMed Scopus Google Scholar, of the larval hemolymph Full Text Full Text PDF PubMed Scopus Google Scholar, R. larval hemolymph protein Res. 2003; PubMed Scopus Google term of to mellifera hemolymph proteins for which are a studies for the major protein with is a of a protein found in fluid and of Full Text Full Text PDF PubMed Scopus Google and the from male of an and of the PubMed Scopus Google Scholar), an in the of to hemolymph to include proteins to are in other caste protein to be in and adult queen and hemolymph contained a protein with a role in hemolymph contained more in than adult for the of and and a better of is the of an in hemolymph. of of be throughout all of so proteins in adult bees as well but at is with which in the of the so this at a of protein for of protein in proteomics the of Full Text Full Text PDF PubMed Scopus Google long as of different is is a for the of proteins in different especially it is to all to the complex data the other protein for a protein found between high of a the and to the for a in a even it is The of this the for a in different will be and so the we proteins for this at in each all other proteins this in have to major as a for and PubMed Scopus Google so we at the with which we to a in one hemolymph and so the bees in the can but the in the to this This hemolymph be a fluid for the of other honeybee with as In are and is for to for even large but be in large as of initial of this study to the molecular components of the honeybee immune system, which is to be to both are the honeybee hemolymph found to at proteins of the and which in to and is a of the against and Simoes Z.L. Bitondi M.M. in Apis mellifera honey bee and expression of the Biochem. PubMed Scopus Google Scholar), a defense to and of in be the of its immune and be at responsible for the of in all larval of the a protein a J.H. a for and the for the of innate immune genes in Full Text Full Text PDF PubMed Scopus Google Scholar, of the 2003; PubMed Scopus Google responsible for the of and R. The in The Scholar), also found in mellifera proteins and found to be to the protein its to the of is for is a PubMed Scopus Google protein be but the protein at all in hemolymph. an and characterization of an is in the honeybee Full Text PDF PubMed Google Scholar), is in in with the protein in to expression of a protein in and of Sci. PubMed Scopus Google and to role of a protein in in of the Full Text Full Text PDF PubMed Scopus Google Scholar), which is a known of the proteins and PubMed Scopus Google The honeybee is a large protein but it is very This other of the protein in the hemolymph but are to In it is adult workers have more proteins with this is the stage and it a for the of to as and proteomics be to hemolymph from studies have in a of and other as and and of the immune of PubMed Scopus Google Scholar, proteomics for Sci. PubMed Scopus Google Scholar, The immune is Res. PubMed Scopus Google Scholar, R. R. of Res. PubMed Scopus Google in studies of in the Biochem. 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