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Using a broad metabolomics approach, we found that GpsA serves as a dominant regulator of NADH and glycerol-3-phosphate levels<jats:italic>in vitro<\/jats:italic>, metabolic intermediates that reflect the cellular redox potential and serve as a precursor for lipid and lipoprotein biosynthesis, respectively. Additionally, GpsA was required for survival under nutrient stress, regulated overall reductase activity and controlled<jats:italic>B<\/jats:italic>.<jats:italic>burgdorferi<\/jats:italic>morphology<jats:italic>in vitro<\/jats:italic>. Furthermore, during<jats:italic>in vitro<\/jats:italic>nutrient stress, both glycerol and<jats:italic>N<\/jats:italic>-acetylglucosamine were bactericidal to<jats:italic>B<\/jats:italic>.<jats:italic>burgdorferi<\/jats:italic>in a GlpD-dependent manner. This study is also the first to identify a suppressor mutation in<jats:italic>B<\/jats:italic>.<jats:italic>burgdorferi<\/jats:italic>: a<jats:italic>glpD<\/jats:italic>deletion restored the wild-type phenotype to the pleiotropic<jats:italic>gpsA<\/jats:italic>mutant, including murine infectivity by needle inoculation at high doses, survival under nutrient stress, morphological changes and the metabolic imbalance of NADH and glycerol-3-phosphate. These results illustrate how basic metabolic functions that are dispensable for<jats:italic>in vitro<\/jats:italic>growth can be essential for<jats:italic>in vivo<\/jats:italic>infectivity of<jats:italic>B<\/jats:italic>.<jats:italic>burgdorferi<\/jats:italic>and may serve as attractive therapeutic targets.<\/jats:p>","DOI":"10.1371\/journal.ppat.1010385","type":"journal-article","created":{"date-parts":[[2022,3,7]],"date-time":"2022-03-07T18:35:56Z","timestamp":1646678156000},"page":"e1010385","update-policy":"https:\/\/doi.org\/10.1371\/journal.ppat.corrections_policy","source":"Crossref","is-referenced-by-count":28,"title":["The glycerol-3-phosphate dehydrogenases GpsA and GlpD constitute the oxidoreductive metabolic linchpin for Lyme disease spirochete host infectivity and persistence in the tick"],"prefix":"10.1371","volume":"18","author":[{"ORCID":"https:\/\/orcid.org\/0000-0001-7090-6236","authenticated-orcid":true,"given":"Dan","family":"Drecktrah","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Laura S.","family":"Hall","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Bethany","family":"Crouse","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Benjamin","family":"Schwarz","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Crystal","family":"Richards","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Eric","family":"Bohrnsen","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Michael","family":"Wulf","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Bonnie","family":"Long","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jessica","family":"Bailey","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Frank","family":"Gherardini","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Catharine M.","family":"Bosio","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Meghan C.","family":"Lybecker","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"D. 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