{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,16]],"date-time":"2026-09-16T16:28:33Z","timestamp":1789576113177,"version":"build-2803163510"},"reference-count":72,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2023,5,24]],"date-time":"2023-05-24T00:00:00Z","timestamp":1684886400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Microbiol."],"abstract":"<jats:sec><jats:title>Introduction<\/jats:title><jats:p>Semen quality is decreasing worldwide, leading to increased male infertility. This study analyzed the microbiota of the gut, semen, and urine in individuals with semen abnormalities to identify potential probiotics and pathogenic bacteria that affect semen parameters and help develop new methods for the diagnosis and treatment of patients with semen abnormalities.<\/jats:p><\/jats:sec><jats:sec><jats:title>Methods<\/jats:title><jats:p>We recruited 12 individuals with normal semen parameters (control group), 12 with asthenospermia but no semen hyperviscosity (Group_1), 6 with oligospermia (Group_2), 9 with severe oligospermia or azoospermia (Group_3), and 14 with semen hyperviscosity only (Group_4). The semen, gut, and urine microbiota were examined by analyzing the 16S ribosomal RNA gene sequence using next-generation sequencing.<\/jats:p><\/jats:sec><jats:sec><jats:title>Results<\/jats:title><jats:p>The gut microbes were clustered into the highest number of operational taxonomic units, followed by urine and semen. Furthermore, the \u03b1-diversity of gut microbes was highest and significantly different from that of urine and semen microbiota. The microbiota of the gut, urine, and semen were all significantly different from each other in terms of \u03b2-diversity. The gut abundance of <jats:italic>Collinsella<\/jats:italic> was significantly reduced in groups 1, 3, and 4. Furthermore, the gut abundance of <jats:italic>Bifidobacterium<\/jats:italic> and <jats:italic>Blautia<\/jats:italic> was significantly decreased in Group_1, while that of <jats:italic>Bacteroides<\/jats:italic> was significantly increased in Group_3. The abundance of <jats:italic>Staphylococcus<\/jats:italic> was significantly increased in the semen of groups 1 and 4. Finally, <jats:italic>Lactobacillus<\/jats:italic> abundance was significantly reduced in the urine of groups 2 and 4.<\/jats:p><\/jats:sec><jats:sec><jats:title>Discussion<\/jats:title><jats:p>This study comprehensively describes the differences in intestinal and genitourinary tract microbiota between healthy individuals and those with abnormal semen parameters. Furthermore, our study identified <jats:italic>Collinsella<\/jats:italic>, <jats:italic>Bifidobacterium<\/jats:italic>, <jats:italic>Blautia<\/jats:italic>, and <jats:italic>Lactobacillus<\/jats:italic> as potential probiotics. Finally, the study identified <jats:italic>Bacteroides<\/jats:italic> in the gut and <jats:italic>Staphylococcus<\/jats:italic> in semen as potential pathogenic bacteria. Our study lays the foundation of a new approach to the diagnosis and treatment of male infertility.<\/jats:p><\/jats:sec>","DOI":"10.3389\/fmicb.2023.1182320","type":"journal-article","created":{"date-parts":[[2023,5,24]],"date-time":"2023-05-24T05:42:27Z","timestamp":1684906947000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":34,"title":["Characterization of the semen, gut, and urine microbiota in patients with different semen abnormalities"],"prefix":"10.3389","volume":"14","author":[{"given":"Tingshuai","family":"Cao","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Shangren","family":"Wang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yang","family":"Pan","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Feng","family":"Guo","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Bin","family":"Wu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yingchun","family":"Zhang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yujie","family":"Wang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jiaqing","family":"Tian","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Qingfei","family":"Xing","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xiaoqiang","family":"Liu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1965","published-online":{"date-parts":[[2023,5,24]]},"reference":[{"key":"ref1","doi-asserted-by":"publisher","first-page":"1174","DOI":"10.1136\/gutjnl-2020-323071","article-title":"Gut microbiota-derived metabolites as central regulators in metabolic disorders","volume":"70","author":"Agus","year":"2021","journal-title":"Gut"},{"key":"ref2","doi-asserted-by":"publisher","first-page":"e103809","DOI":"10.1371\/journal.pone.0103809","article-title":"The gut microbiota and developmental programming of the testis in mice","volume":"9","author":"Al-Asmakh","year":"2014","journal-title":"PLoS One"},{"key":"ref3","doi-asserted-by":"publisher","first-page":"1212","DOI":"10.1093\/humrep\/dey116","article-title":"Testicular microbiome in azoospermic men-first evidence of the impact of an altered microenvironment","volume":"33","author":"Alfano","year":"2018","journal-title":"Hum. 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A."},{"key":"ref15","doi-asserted-by":"publisher","first-page":"D141","DOI":"10.1093\/nar\/gkn879","article-title":"The ribosomal database project: improved alignments and new tools for rRNA analysis","volume":"37","author":"Cole","year":"2009","journal-title":"Nucleic Acids Res."},{"key":"ref16","doi-asserted-by":"publisher","first-page":"389","DOI":"10.1093\/molehr\/gav003","article-title":"Amino acid metabolism in intestinal bacteria and its potential implications for mammalian reproduction","volume":"21","author":"Dai","year":"2015","journal-title":"Mol. Hum. Reprod."},{"key":"ref17","doi-asserted-by":"publisher","first-page":"1768","DOI":"10.2741\/3820","article-title":"Amino acid metabolism in intestinal bacteria: links between gut ecology and host health","volume":"16","author":"Dai","year":"2011","journal-title":"Front. Biosci. 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Spectr."},{"key":"ref30","doi-asserted-by":"publisher","first-page":"45","DOI":"10.1186\/s10020-022-00473-w","article-title":"Gut microbiota-testis axis: FMT improves systemic and testicular micro-environment to increase semen quality in type 1 diabetes","volume":"28","author":"Hao","year":"","journal-title":"Mol. Med."},{"key":"ref31","doi-asserted-by":"publisher","first-page":"e0260451","DOI":"10.1371\/journal.pone.0260451","article-title":"Intestinal collinsella may mitigate infection and exacerbation of COVID-19 by producing ursodeoxycholate","volume":"16","author":"Hirayama","year":"2021","journal-title":"PLoS One"},{"key":"ref32","doi-asserted-by":"publisher","first-page":"1261","DOI":"10.1016\/j.fertnstert.2013.07.1991","article-title":"Microbiota of the seminal fluid from healthy and infertile men","volume":"100","author":"Hou","year":"2013","journal-title":"Fertil. Steril."},{"key":"ref33","doi-asserted-by":"publisher","first-page":"235","DOI":"10.1186\/s40168-021-01181-z","article-title":"Regulation of blood-brain barrier integrity by microbiome-associated methylamines and cognition by trimethylamine N-oxide","volume":"9","author":"Hoyles","year":"2021","journal-title":"Microbiome"},{"key":"ref34","doi-asserted-by":"publisher","first-page":"1069","DOI":"10.1038\/ismej.2013.2","article-title":"Exploring the bovine rumen bacterial community from birth to adulthood","volume":"7","author":"Jami","year":"2013","journal-title":"ISME J."},{"key":"ref35","first-page":"21","article-title":"Obstructive azoospermia: a study of 102 patients","volume":"3","author":"Jequier","year":"1985","journal-title":"Clin. Reprod. Fertil."},{"key":"ref36","doi-asserted-by":"publisher","first-page":"4650","DOI":"10.1128\/AEM.02599-07","article-title":"Oral administration of Lactobacillus strains isolated from breast milk as an alternative for the treatment of infectious mastitis during lactation","volume":"74","author":"Jimenez","year":"2008","journal-title":"Appl. Environ. Microbiol."},{"key":"ref37","doi-asserted-by":"publisher","first-page":"5821","DOI":"10.1038\/s41598-019-42183-0","article-title":"Long-term benefit of microbiota transfer therapy on autism symptoms and gut microbiota","volume":"9","author":"Kang","year":"2019","journal-title":"Sci. Rep."},{"key":"ref38","doi-asserted-by":"publisher","first-page":"10","DOI":"10.1186\/s40168-016-0225-7","article-title":"Microbiota transfer therapy alters gut ecosystem and improves gastrointestinal and autism symptoms: an open-label study","volume":"5","author":"Kang","year":"2017","journal-title":"Microbiome"},{"key":"ref39","doi-asserted-by":"publisher","first-page":"277","DOI":"10.4110\/in.2014.14.6.277","article-title":"Gut microbiota-derived short-chain fatty acids, T cells, and inflammation","volume":"14","author":"Kim","year":"2014","journal-title":"Immune Netw."},{"key":"ref40","doi-asserted-by":"publisher","first-page":"1829","DOI":"10.1038\/ncomms2852","article-title":"The gut microbiota suppresses insulin-mediated fat accumulation via the short-chain fatty acid receptor GPR43","volume":"4","author":"Kimura","year":"2013","journal-title":"Nat. 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Total Environ."},{"key":"ref44","doi-asserted-by":"publisher","first-page":"818","DOI":"10.1016\/j.tem.2020.02.012","article-title":"Gut microbial metabolites of aromatic amino acids as signals in host-microbe interplay","volume":"31","author":"Liu","year":"2020","journal-title":"Trends Endocrinol. Metab."},{"key":"ref45","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1080\/19490976.2021.1903826","article-title":"Blautia-a new functional genus with potential probiotic properties?","volume":"13","author":"Liu","year":"2021","journal-title":"Gut Microbes"},{"key":"ref46","doi-asserted-by":"publisher","first-page":"826","DOI":"10.1016\/j.eururo.2021.01.014","article-title":"Functional and taxonomic dysbiosis of the gut, urine, and semen microbiomes in male infertility","volume":"79","author":"Lundy","year":"2021","journal-title":"Eur. Urol."},{"key":"ref47","doi-asserted-by":"publisher","first-page":"888023","DOI":"10.3389\/fvets.2022.888023","article-title":"Commensal lactobacilli enhance sperm qualitative parameters in dogs","volume":"9","author":"Mahiddine","year":"2022","journal-title":"Front. Vet. Sci."},{"key":"ref48","doi-asserted-by":"publisher","first-page":"299","DOI":"10.1590\/S1677-55382009000300006","article-title":"Impact of infection on the secretory capacity of the male accessory glands","volume":"35","author":"Marconi","year":"2009","journal-title":"Int. Braz. J. 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Steril."},{"key":"ref60","doi-asserted-by":"publisher","first-page":"3621","DOI":"10.1038\/s41467-019-11460-x","article-title":"Genetic risk for autoimmunity is associated with distinct changes in the human gut microbiome","volume":"10","author":"Russell","year":"2019","journal-title":"Nat. Commun."},{"key":"ref61","doi-asserted-by":"publisher","first-page":"39","DOI":"10.1093\/humupd\/dmh003","article-title":"Role of caspases in male infertility","volume":"10","author":"Said","year":"2004","journal-title":"Hum. Reprod. Update"},{"key":"ref62","doi-asserted-by":"publisher","first-page":"247","DOI":"10.1177\/0960327117703690","article-title":"Decline in sperm count in European men during the past 50 years","volume":"37","author":"Sengupta","year":"2018","journal-title":"Hum. Exp. 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