The impact of pollen consumption on honey bee (Apis mellifera) digestive physiology and carbohydrate metabolism
Carbohydrate‐active enzymes play an important role in the honey bee (Apis mellifera) due to its dietary specialization on plant‐based nutrition. Secretory glycoside hydrolases (GHs) produced in worker head glands aid in the processing of floral nectar into honey and are expressed in accordance with...
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| Veröffentlicht in: | Archives of insect biochemistry and physiology 2017-10, Vol.96 (2), p.n/a |
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| container_title | Archives of insect biochemistry and physiology |
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| creator | Ricigliano, Vincent A. Fitz, William Copeland, Duan C. Mott, Brendon M. Maes, Patrick Floyd, Amy S. Dockstader, Arnold Anderson, Kirk E. |
| description | Carbohydrate‐active enzymes play an important role in the honey bee (Apis mellifera) due to its dietary specialization on plant‐based nutrition. Secretory glycoside hydrolases (GHs) produced in worker head glands aid in the processing of floral nectar into honey and are expressed in accordance with age‐based division of labor. Pollen utilization by the honey bee has been investigated in considerable detail, but little is known about the metabolic fate of indigestible carbohydrates and glycosides in pollen biomass. Here, we demonstrate that pollen consumption stimulates the hydrolysis of sugars that are toxic to the bee (xylose, arabinose, mannose). GHs produced in the head accumulate in the midgut and persist in the hindgut that harbors a core microbial community composed of approximately 108 bacterial cells. Pollen consumption significantly impacted total and specific bacterial abundance in the digestive tract. Bacterial isolates representing major fermentative gut phylotypes exhibited primarily membrane‐bound GH activities that may function in tandem with soluble host enzymes retained in the hindgut. Additionally, we found that plant‐originating β‐galactosidase activity in pollen may be sufficient, in some cases, for probable physiological activity in the gut. These findings emphasize the potential relative contributions of host, bacteria, and pollen enzyme activities to carbohydrate breakdown, which may be tied to gut microbiome dynamics and associated host nutrition. |
| doi_str_mv | 10.1002/arch.21406 |
| format | Article |
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Secretory glycoside hydrolases (GHs) produced in worker head glands aid in the processing of floral nectar into honey and are expressed in accordance with age‐based division of labor. Pollen utilization by the honey bee has been investigated in considerable detail, but little is known about the metabolic fate of indigestible carbohydrates and glycosides in pollen biomass. Here, we demonstrate that pollen consumption stimulates the hydrolysis of sugars that are toxic to the bee (xylose, arabinose, mannose). GHs produced in the head accumulate in the midgut and persist in the hindgut that harbors a core microbial community composed of approximately 108 bacterial cells. Pollen consumption significantly impacted total and specific bacterial abundance in the digestive tract. Bacterial isolates representing major fermentative gut phylotypes exhibited primarily membrane‐bound GH activities that may function in tandem with soluble host enzymes retained in the hindgut. Additionally, we found that plant‐originating β‐galactosidase activity in pollen may be sufficient, in some cases, for probable physiological activity in the gut. These findings emphasize the potential relative contributions of host, bacteria, and pollen enzyme activities to carbohydrate breakdown, which may be tied to gut microbiome dynamics and associated host nutrition.</description><identifier>ISSN: 0739-4462</identifier><identifier>EISSN: 1520-6327</identifier><identifier>DOI: 10.1002/arch.21406</identifier><identifier>PMID: 28833462</identifier><language>eng</language><publisher>United States: Wiley Subscription Services, Inc</publisher><subject>Abundance ; Age ; Animals ; Apis mellifera ; Arabinose ; Bacteria ; Bees ; Bees - microbiology ; Bees - physiology ; beta-galactosidase ; Biomass ; Carbohydrate Metabolism ; Carbohydrates ; Consumption ; Digestion ; digestive physiology ; Digestive system ; digestive tract ; Division of labor ; enzyme activity ; Enzymes ; Flowers ; Galactosidase ; Gastrointestinal tract ; Gastrointestinal Tract - microbiology ; Glands ; Glycoside hydrolase ; Glycoside Hydrolases - metabolism ; Glycosides ; head ; Hindgut ; Honey ; honey bee (Apis mellifera) ; honey bees ; Host plants ; hydrolysis ; Intestinal microflora ; intestinal microorganisms ; Mannose ; Metabolism ; microbial communities ; Microbiota ; Microorganisms ; Midgut ; Nectar ; Nutrition ; phylotype ; Pollen ; polyethism ; Sugar ; toxicity ; Xylose ; β-Galactosidase</subject><ispartof>Archives of insect biochemistry and physiology, 2017-10, Vol.96 (2), p.n/a</ispartof><rights>2017 Wiley Periodicals, Inc.</rights><rights>Copyright © 2017 Wiley Periodicals, Inc.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c4266-ee8b842cf42a3f3192a4c10ee1aa6716fc8638dfa36275e4a0281bfc058850a33</citedby><cites>FETCH-LOGICAL-c4266-ee8b842cf42a3f3192a4c10ee1aa6716fc8638dfa36275e4a0281bfc058850a33</cites><orcidid>0000-0002-5167-5812</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1002%2Farch.21406$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1002%2Farch.21406$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>314,776,780,1411,27903,27904,45553,45554</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/28833462$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Ricigliano, Vincent A.</creatorcontrib><creatorcontrib>Fitz, William</creatorcontrib><creatorcontrib>Copeland, Duan C.</creatorcontrib><creatorcontrib>Mott, Brendon M.</creatorcontrib><creatorcontrib>Maes, Patrick</creatorcontrib><creatorcontrib>Floyd, Amy S.</creatorcontrib><creatorcontrib>Dockstader, Arnold</creatorcontrib><creatorcontrib>Anderson, Kirk E.</creatorcontrib><title>The impact of pollen consumption on honey bee (Apis mellifera) digestive physiology and carbohydrate metabolism</title><title>Archives of insect biochemistry and physiology</title><addtitle>Arch Insect Biochem Physiol</addtitle><description>Carbohydrate‐active enzymes play an important role in the honey bee (Apis mellifera) due to its dietary specialization on plant‐based nutrition. Secretory glycoside hydrolases (GHs) produced in worker head glands aid in the processing of floral nectar into honey and are expressed in accordance with age‐based division of labor. Pollen utilization by the honey bee has been investigated in considerable detail, but little is known about the metabolic fate of indigestible carbohydrates and glycosides in pollen biomass. Here, we demonstrate that pollen consumption stimulates the hydrolysis of sugars that are toxic to the bee (xylose, arabinose, mannose). GHs produced in the head accumulate in the midgut and persist in the hindgut that harbors a core microbial community composed of approximately 108 bacterial cells. Pollen consumption significantly impacted total and specific bacterial abundance in the digestive tract. Bacterial isolates representing major fermentative gut phylotypes exhibited primarily membrane‐bound GH activities that may function in tandem with soluble host enzymes retained in the hindgut. Additionally, we found that plant‐originating β‐galactosidase activity in pollen may be sufficient, in some cases, for probable physiological activity in the gut. These findings emphasize the potential relative contributions of host, bacteria, and pollen enzyme activities to carbohydrate breakdown, which may be tied to gut microbiome dynamics and associated host nutrition.</description><subject>Abundance</subject><subject>Age</subject><subject>Animals</subject><subject>Apis mellifera</subject><subject>Arabinose</subject><subject>Bacteria</subject><subject>Bees</subject><subject>Bees - microbiology</subject><subject>Bees - physiology</subject><subject>beta-galactosidase</subject><subject>Biomass</subject><subject>Carbohydrate Metabolism</subject><subject>Carbohydrates</subject><subject>Consumption</subject><subject>Digestion</subject><subject>digestive physiology</subject><subject>Digestive system</subject><subject>digestive tract</subject><subject>Division of labor</subject><subject>enzyme activity</subject><subject>Enzymes</subject><subject>Flowers</subject><subject>Galactosidase</subject><subject>Gastrointestinal tract</subject><subject>Gastrointestinal Tract - microbiology</subject><subject>Glands</subject><subject>Glycoside hydrolase</subject><subject>Glycoside Hydrolases - metabolism</subject><subject>Glycosides</subject><subject>head</subject><subject>Hindgut</subject><subject>Honey</subject><subject>honey bee (Apis mellifera)</subject><subject>honey bees</subject><subject>Host plants</subject><subject>hydrolysis</subject><subject>Intestinal microflora</subject><subject>intestinal microorganisms</subject><subject>Mannose</subject><subject>Metabolism</subject><subject>microbial communities</subject><subject>Microbiota</subject><subject>Microorganisms</subject><subject>Midgut</subject><subject>Nectar</subject><subject>Nutrition</subject><subject>phylotype</subject><subject>Pollen</subject><subject>polyethism</subject><subject>Sugar</subject><subject>toxicity</subject><subject>Xylose</subject><subject>β-Galactosidase</subject><issn>0739-4462</issn><issn>1520-6327</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2017</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp9kVFr1jAUhoMo7nN64w-QgDdT6DxJ2jS9_PhQNxgIY16HND1ZM9qmJu2k_95s3_TCi8GBwOHJw8t5CXnP4JwB8C8m2v6csxLkC7JjFYdCCl6_JDuoRVOUpeQn5E1KdwDQSKZekxOulBB5vyPhpkfqx9nYhQZH5zAMOFEbprSO8-LDRPP0YcKNtoj0bD_7REccBu8wmk-087eYFn-PdO635MMQbjdqpo5aE9vQb100C-YPi2nD4NP4lrxyZkj47uk9JT-_fb05XBRXP75fHvZXhS25lAWialXJrSu5EU6whpvSMkBkxsiaSWeVFKpzRkheV1ga4Iq1zkKlVAVGiFNydvTOMfxac0Q9-mRzbjNhWJPmUFYKRC2qjH78D70La5xyOs0aUVcNgGKZ-nykbAwpRXR6jn40cdMM9EMN-qEG_VhDhj88Kdd2xO4f-vfuGWBH4LcfcHtGpffXh4uj9A8f-pKa</recordid><startdate>201710</startdate><enddate>201710</enddate><creator>Ricigliano, Vincent A.</creator><creator>Fitz, William</creator><creator>Copeland, Duan C.</creator><creator>Mott, Brendon M.</creator><creator>Maes, Patrick</creator><creator>Floyd, Amy S.</creator><creator>Dockstader, Arnold</creator><creator>Anderson, Kirk E.</creator><general>Wiley Subscription Services, Inc</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7QR</scope><scope>7SS</scope><scope>7U9</scope><scope>8FD</scope><scope>FR3</scope><scope>H94</scope><scope>P64</scope><scope>RC3</scope><scope>7S9</scope><scope>L.6</scope><orcidid>https://orcid.org/0000-0002-5167-5812</orcidid></search><sort><creationdate>201710</creationdate><title>The impact of pollen consumption on honey bee (Apis mellifera) digestive physiology and carbohydrate metabolism</title><author>Ricigliano, Vincent A. ; Fitz, William ; Copeland, Duan C. ; Mott, Brendon M. ; Maes, Patrick ; Floyd, Amy S. ; Dockstader, Arnold ; Anderson, Kirk E.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c4266-ee8b842cf42a3f3192a4c10ee1aa6716fc8638dfa36275e4a0281bfc058850a33</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2017</creationdate><topic>Abundance</topic><topic>Age</topic><topic>Animals</topic><topic>Apis mellifera</topic><topic>Arabinose</topic><topic>Bacteria</topic><topic>Bees</topic><topic>Bees - microbiology</topic><topic>Bees - physiology</topic><topic>beta-galactosidase</topic><topic>Biomass</topic><topic>Carbohydrate Metabolism</topic><topic>Carbohydrates</topic><topic>Consumption</topic><topic>Digestion</topic><topic>digestive physiology</topic><topic>Digestive system</topic><topic>digestive tract</topic><topic>Division of labor</topic><topic>enzyme activity</topic><topic>Enzymes</topic><topic>Flowers</topic><topic>Galactosidase</topic><topic>Gastrointestinal tract</topic><topic>Gastrointestinal Tract - microbiology</topic><topic>Glands</topic><topic>Glycoside hydrolase</topic><topic>Glycoside Hydrolases - metabolism</topic><topic>Glycosides</topic><topic>head</topic><topic>Hindgut</topic><topic>Honey</topic><topic>honey bee (Apis mellifera)</topic><topic>honey bees</topic><topic>Host plants</topic><topic>hydrolysis</topic><topic>Intestinal microflora</topic><topic>intestinal microorganisms</topic><topic>Mannose</topic><topic>Metabolism</topic><topic>microbial communities</topic><topic>Microbiota</topic><topic>Microorganisms</topic><topic>Midgut</topic><topic>Nectar</topic><topic>Nutrition</topic><topic>phylotype</topic><topic>Pollen</topic><topic>polyethism</topic><topic>Sugar</topic><topic>toxicity</topic><topic>Xylose</topic><topic>β-Galactosidase</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Ricigliano, Vincent A.</creatorcontrib><creatorcontrib>Fitz, William</creatorcontrib><creatorcontrib>Copeland, Duan C.</creatorcontrib><creatorcontrib>Mott, Brendon M.</creatorcontrib><creatorcontrib>Maes, Patrick</creatorcontrib><creatorcontrib>Floyd, Amy S.</creatorcontrib><creatorcontrib>Dockstader, Arnold</creatorcontrib><creatorcontrib>Anderson, Kirk E.</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Chemoreception Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Virology and AIDS Abstracts</collection><collection>Technology Research Database</collection><collection>Engineering Research Database</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>AGRICOLA</collection><collection>AGRICOLA - Academic</collection><jtitle>Archives of insect biochemistry and physiology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Ricigliano, Vincent A.</au><au>Fitz, William</au><au>Copeland, Duan C.</au><au>Mott, Brendon M.</au><au>Maes, Patrick</au><au>Floyd, Amy S.</au><au>Dockstader, Arnold</au><au>Anderson, Kirk E.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>The impact of pollen consumption on honey bee (Apis mellifera) digestive physiology and carbohydrate metabolism</atitle><jtitle>Archives of insect biochemistry and physiology</jtitle><addtitle>Arch Insect Biochem Physiol</addtitle><date>2017-10</date><risdate>2017</risdate><volume>96</volume><issue>2</issue><epage>n/a</epage><issn>0739-4462</issn><eissn>1520-6327</eissn><abstract>Carbohydrate‐active enzymes play an important role in the honey bee (Apis mellifera) due to its dietary specialization on plant‐based nutrition. Secretory glycoside hydrolases (GHs) produced in worker head glands aid in the processing of floral nectar into honey and are expressed in accordance with age‐based division of labor. Pollen utilization by the honey bee has been investigated in considerable detail, but little is known about the metabolic fate of indigestible carbohydrates and glycosides in pollen biomass. Here, we demonstrate that pollen consumption stimulates the hydrolysis of sugars that are toxic to the bee (xylose, arabinose, mannose). GHs produced in the head accumulate in the midgut and persist in the hindgut that harbors a core microbial community composed of approximately 108 bacterial cells. Pollen consumption significantly impacted total and specific bacterial abundance in the digestive tract. Bacterial isolates representing major fermentative gut phylotypes exhibited primarily membrane‐bound GH activities that may function in tandem with soluble host enzymes retained in the hindgut. Additionally, we found that plant‐originating β‐galactosidase activity in pollen may be sufficient, in some cases, for probable physiological activity in the gut. These findings emphasize the potential relative contributions of host, bacteria, and pollen enzyme activities to carbohydrate breakdown, which may be tied to gut microbiome dynamics and associated host nutrition.</abstract><cop>United States</cop><pub>Wiley Subscription Services, Inc</pub><pmid>28833462</pmid><doi>10.1002/arch.21406</doi><tpages>14</tpages><orcidid>https://orcid.org/0000-0002-5167-5812</orcidid><oa>free_for_read</oa></addata></record> |
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| subjects | Abundance Age Animals Apis mellifera Arabinose Bacteria Bees Bees - microbiology Bees - physiology beta-galactosidase Biomass Carbohydrate Metabolism Carbohydrates Consumption Digestion digestive physiology Digestive system digestive tract Division of labor enzyme activity Enzymes Flowers Galactosidase Gastrointestinal tract Gastrointestinal Tract - microbiology Glands Glycoside hydrolase Glycoside Hydrolases - metabolism Glycosides head Hindgut Honey honey bee (Apis mellifera) honey bees Host plants hydrolysis Intestinal microflora intestinal microorganisms Mannose Metabolism microbial communities Microbiota Microorganisms Midgut Nectar Nutrition phylotype Pollen polyethism Sugar toxicity Xylose β-Galactosidase |
| title | The impact of pollen consumption on honey bee (Apis mellifera) digestive physiology and carbohydrate metabolism |
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