The microbial metagenome and bone tissue composition in mice with microbiome-induced reductions in bone strength
The genetic components of microbial species that inhabit the body are known collectively as the microbiome. Modifications to the microbiome have been implicated in disease processes throughout the body and have recently been shown to influence bone. Prior work has associated changes in the microbial...
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| Veröffentlicht in: | Bone (New York, N.Y.) N.Y.), 2019-10, Vol.127, p.146-154 |
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| creator | Guss, Jason D. Taylor, Erik Rouse, Zach Roubert, Sebastian Higgins, Catherine H. Thomas, Corinne J. Baker, Shefford P. Vashishth, Deepak Donnelly, Eve Shea, M. Kyla Booth, Sarah L. Bicalho, Rodrigo C. Hernandez, Christopher J. |
| description | The genetic components of microbial species that inhabit the body are known collectively as the microbiome. Modifications to the microbiome have been implicated in disease processes throughout the body and have recently been shown to influence bone. Prior work has associated changes in the microbial taxonomy (phyla, class, species, etc.) in the gut with bone phenotypes but has provided limited information regarding mechanisms. With the goal of achieving a more mechanistic understanding of the effects of the microbiome on bone, we perform a metagenomic analysis of the gut microbiome that provides information on the functional capacity of the microbes (all microbial genes present) rather than only characterizing the microbial taxa. Male C57Bl/6 mice were subjected to disruption of the gut microbiota (ΔMicrobiome) using oral antibiotics (from 4 to 16 weeks of age) or remained untreated (n = 6–7/group). Disruption of the gut microbiome in this manner has been shown to lead to reductions in tissue mechanical properties and whole bone strength in adulthood with only minor changes in bone geometry and density. ΔMicrobiome led to modifications in the abundance of microbial genes responsible for the synthesis of the bacterial cell wall and capsule; bacterially synthesized carbohydrates; and bacterially synthesized vitamins (B and K) (p |
| doi_str_mv | 10.1016/j.bone.2019.06.010 |
| format | Article |
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•Microbiome-induced reductions in bone tissue strength associated with changes in vitamin production by gut microbes•Microbe-derived vitamin K is depleted in mice with impaired bone strength.•Reduced vitamin K and bone strength is associated with bone matrix crystallinity.•Vitamin K production by gut microbes may influence bone quality.</description><identifier>ISSN: 8756-3282</identifier><identifier>EISSN: 1873-2763</identifier><identifier>DOI: 10.1016/j.bone.2019.06.010</identifier><identifier>PMID: 31207357</identifier><language>eng</language><publisher>United States: Elsevier Inc</publisher><subject>adulthood ; bacteria ; Biomechanics ; bone health ; Bone matrix ; bone strength ; bones ; cecum ; cell walls ; crystal structure ; geometry ; intestinal microorganisms ; liver ; males ; menaquinones ; metagenomics ; Microbiome ; Osteoimmunology ; Osteoporosis ; Raman spectroscopy ; taxonomy</subject><ispartof>Bone (New York, N.Y.), 2019-10, Vol.127, p.146-154</ispartof><rights>2019 Elsevier Inc.</rights><rights>Copyright © 2019 Elsevier Inc. All rights reserved.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c488t-22c7c521ef1bb2dbbfcb1a5881821f505c6dfcc9a9f786ea5b89397c53af49393</citedby><cites>FETCH-LOGICAL-c488t-22c7c521ef1bb2dbbfcb1a5881821f505c6dfcc9a9f786ea5b89397c53af49393</cites><orcidid>0000-0002-0712-6533</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://www.sciencedirect.com/science/article/pii/S875632821930242X$$EHTML$$P50$$Gelsevier$$H</linktohtml><link.rule.ids>230,314,776,780,881,3537,27901,27902,65534</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/31207357$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Guss, Jason D.</creatorcontrib><creatorcontrib>Taylor, Erik</creatorcontrib><creatorcontrib>Rouse, Zach</creatorcontrib><creatorcontrib>Roubert, Sebastian</creatorcontrib><creatorcontrib>Higgins, Catherine H.</creatorcontrib><creatorcontrib>Thomas, Corinne J.</creatorcontrib><creatorcontrib>Baker, Shefford P.</creatorcontrib><creatorcontrib>Vashishth, Deepak</creatorcontrib><creatorcontrib>Donnelly, Eve</creatorcontrib><creatorcontrib>Shea, M. Kyla</creatorcontrib><creatorcontrib>Booth, Sarah L.</creatorcontrib><creatorcontrib>Bicalho, Rodrigo C.</creatorcontrib><creatorcontrib>Hernandez, Christopher J.</creatorcontrib><title>The microbial metagenome and bone tissue composition in mice with microbiome-induced reductions in bone strength</title><title>Bone (New York, N.Y.)</title><addtitle>Bone</addtitle><description>The genetic components of microbial species that inhabit the body are known collectively as the microbiome. Modifications to the microbiome have been implicated in disease processes throughout the body and have recently been shown to influence bone. Prior work has associated changes in the microbial taxonomy (phyla, class, species, etc.) in the gut with bone phenotypes but has provided limited information regarding mechanisms. With the goal of achieving a more mechanistic understanding of the effects of the microbiome on bone, we perform a metagenomic analysis of the gut microbiome that provides information on the functional capacity of the microbes (all microbial genes present) rather than only characterizing the microbial taxa. Male C57Bl/6 mice were subjected to disruption of the gut microbiota (ΔMicrobiome) using oral antibiotics (from 4 to 16 weeks of age) or remained untreated (n = 6–7/group). Disruption of the gut microbiome in this manner has been shown to lead to reductions in tissue mechanical properties and whole bone strength in adulthood with only minor changes in bone geometry and density. ΔMicrobiome led to modifications in the abundance of microbial genes responsible for the synthesis of the bacterial cell wall and capsule; bacterially synthesized carbohydrates; and bacterially synthesized vitamins (B and K) (p < 0.01). Follow up analysis focused on vitamin K, a factor that has previously been associated with bone health. The vitamin K content of the cecum, liver and kidneys was primarily microbe-derived forms of vitamin K (menaquinones) and was decreased by 32–66% in ∆Microbiome mice compared to untreated animals (p < 0.01). Bone mineral crystallinity determined using Raman spectroscopy was decreased in ∆Microbiome mice (p = 0.01). This study illustrates the use of metagenomic analysis to link the microbiome to bone phenotypes and provides preliminary findings implicating microbially synthesized vitamin-K as a regulator of bone matrix quality.
•Microbiome-induced reductions in bone tissue strength associated with changes in vitamin production by gut microbes•Microbe-derived vitamin K is depleted in mice with impaired bone strength.•Reduced vitamin K and bone strength is associated with bone matrix crystallinity.•Vitamin K production by gut microbes may influence bone quality.</description><subject>adulthood</subject><subject>bacteria</subject><subject>Biomechanics</subject><subject>bone health</subject><subject>Bone matrix</subject><subject>bone strength</subject><subject>bones</subject><subject>cecum</subject><subject>cell walls</subject><subject>crystal structure</subject><subject>geometry</subject><subject>intestinal microorganisms</subject><subject>liver</subject><subject>males</subject><subject>menaquinones</subject><subject>metagenomics</subject><subject>Microbiome</subject><subject>Osteoimmunology</subject><subject>Osteoporosis</subject><subject>Raman spectroscopy</subject><subject>taxonomy</subject><issn>8756-3282</issn><issn>1873-2763</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2019</creationdate><recordtype>article</recordtype><recordid>eNqFkUtv1DAUhS1ERYfCH2CBsmST4Mf4EQkhoYqXVKmbdm3Zzs2MR4k92E4R_x6n01awgdW9kr9z5HsOQm8I7ggm4v2hszFARzHpOyw6TPAztCFKspZKwZ6jjZJctIwqeo5e5nzAGLNekhfonBGKJeNyg443e2hm71K03kzNDMXsIMQZGhOGZvVvis95gcbF-RizLz6GxodVA81PX_aP6qppfRgWB0OToM6VzCt675JLgrAr-1fobDRThtcP8wLdfvl8c_mtvbr--v3y01XrtkqVllInHacERmItHawdnSWGK0UUJSPH3IlhdK43_SiVAMOt6utxjjMzbuvGLtDHk-9xsTMMDkJJZtLH5GeTfulovP77Jfi93sU7LSSuua0G7x4MUvyxQC569tnBNJkAccmaCia2gmDM_4_SLVWE95hVlJ7QmlnOCcanHxGs11b1Qa956bVVjYWurVbR2z9veZI81liBDycAaqJ3HpLOzkOoVfgErugh-n_5_wYew7ba</recordid><startdate>20191001</startdate><enddate>20191001</enddate><creator>Guss, Jason D.</creator><creator>Taylor, Erik</creator><creator>Rouse, Zach</creator><creator>Roubert, Sebastian</creator><creator>Higgins, Catherine H.</creator><creator>Thomas, Corinne J.</creator><creator>Baker, Shefford P.</creator><creator>Vashishth, Deepak</creator><creator>Donnelly, Eve</creator><creator>Shea, M. 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Kyla ; Booth, Sarah L. ; Bicalho, Rodrigo C. ; Hernandez, Christopher J.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c488t-22c7c521ef1bb2dbbfcb1a5881821f505c6dfcc9a9f786ea5b89397c53af49393</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2019</creationdate><topic>adulthood</topic><topic>bacteria</topic><topic>Biomechanics</topic><topic>bone health</topic><topic>Bone matrix</topic><topic>bone strength</topic><topic>bones</topic><topic>cecum</topic><topic>cell walls</topic><topic>crystal structure</topic><topic>geometry</topic><topic>intestinal microorganisms</topic><topic>liver</topic><topic>males</topic><topic>menaquinones</topic><topic>metagenomics</topic><topic>Microbiome</topic><topic>Osteoimmunology</topic><topic>Osteoporosis</topic><topic>Raman spectroscopy</topic><topic>taxonomy</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Guss, Jason D.</creatorcontrib><creatorcontrib>Taylor, Erik</creatorcontrib><creatorcontrib>Rouse, Zach</creatorcontrib><creatorcontrib>Roubert, Sebastian</creatorcontrib><creatorcontrib>Higgins, Catherine H.</creatorcontrib><creatorcontrib>Thomas, Corinne J.</creatorcontrib><creatorcontrib>Baker, Shefford P.</creatorcontrib><creatorcontrib>Vashishth, Deepak</creatorcontrib><creatorcontrib>Donnelly, Eve</creatorcontrib><creatorcontrib>Shea, M. Kyla</creatorcontrib><creatorcontrib>Booth, Sarah L.</creatorcontrib><creatorcontrib>Bicalho, Rodrigo C.</creatorcontrib><creatorcontrib>Hernandez, Christopher J.</creatorcontrib><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>AGRICOLA</collection><collection>AGRICOLA - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Bone (New York, N.Y.)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Guss, Jason D.</au><au>Taylor, Erik</au><au>Rouse, Zach</au><au>Roubert, Sebastian</au><au>Higgins, Catherine H.</au><au>Thomas, Corinne J.</au><au>Baker, Shefford P.</au><au>Vashishth, Deepak</au><au>Donnelly, Eve</au><au>Shea, M. Kyla</au><au>Booth, Sarah L.</au><au>Bicalho, Rodrigo C.</au><au>Hernandez, Christopher J.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>The microbial metagenome and bone tissue composition in mice with microbiome-induced reductions in bone strength</atitle><jtitle>Bone (New York, N.Y.)</jtitle><addtitle>Bone</addtitle><date>2019-10-01</date><risdate>2019</risdate><volume>127</volume><spage>146</spage><epage>154</epage><pages>146-154</pages><issn>8756-3282</issn><eissn>1873-2763</eissn><abstract>The genetic components of microbial species that inhabit the body are known collectively as the microbiome. Modifications to the microbiome have been implicated in disease processes throughout the body and have recently been shown to influence bone. Prior work has associated changes in the microbial taxonomy (phyla, class, species, etc.) in the gut with bone phenotypes but has provided limited information regarding mechanisms. With the goal of achieving a more mechanistic understanding of the effects of the microbiome on bone, we perform a metagenomic analysis of the gut microbiome that provides information on the functional capacity of the microbes (all microbial genes present) rather than only characterizing the microbial taxa. Male C57Bl/6 mice were subjected to disruption of the gut microbiota (ΔMicrobiome) using oral antibiotics (from 4 to 16 weeks of age) or remained untreated (n = 6–7/group). Disruption of the gut microbiome in this manner has been shown to lead to reductions in tissue mechanical properties and whole bone strength in adulthood with only minor changes in bone geometry and density. ΔMicrobiome led to modifications in the abundance of microbial genes responsible for the synthesis of the bacterial cell wall and capsule; bacterially synthesized carbohydrates; and bacterially synthesized vitamins (B and K) (p < 0.01). Follow up analysis focused on vitamin K, a factor that has previously been associated with bone health. The vitamin K content of the cecum, liver and kidneys was primarily microbe-derived forms of vitamin K (menaquinones) and was decreased by 32–66% in ∆Microbiome mice compared to untreated animals (p < 0.01). Bone mineral crystallinity determined using Raman spectroscopy was decreased in ∆Microbiome mice (p = 0.01). This study illustrates the use of metagenomic analysis to link the microbiome to bone phenotypes and provides preliminary findings implicating microbially synthesized vitamin-K as a regulator of bone matrix quality.
•Microbiome-induced reductions in bone tissue strength associated with changes in vitamin production by gut microbes•Microbe-derived vitamin K is depleted in mice with impaired bone strength.•Reduced vitamin K and bone strength is associated with bone matrix crystallinity.•Vitamin K production by gut microbes may influence bone quality.</abstract><cop>United States</cop><pub>Elsevier Inc</pub><pmid>31207357</pmid><doi>10.1016/j.bone.2019.06.010</doi><tpages>9</tpages><orcidid>https://orcid.org/0000-0002-0712-6533</orcidid><oa>free_for_read</oa></addata></record> |
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| source | Elsevier ScienceDirect Journals Complete |
| subjects | adulthood bacteria Biomechanics bone health Bone matrix bone strength bones cecum cell walls crystal structure geometry intestinal microorganisms liver males menaquinones metagenomics Microbiome Osteoimmunology Osteoporosis Raman spectroscopy taxonomy |
| title | The microbial metagenome and bone tissue composition in mice with microbiome-induced reductions in bone strength |
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