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Lyme disease and relapsing fever Borrelia elongate through zones of peptidoglycan synthesis that mark division sites of daughter cells
Agents that cause Lyme disease, relapsing fever, leptospirosis, and syphilis belong to the phylum Spirochaetae—a unique lineage of bacteria most known for their long, spiral morphology. Despite the relevance to human health, little is known about the most fundamental aspects of spirochete growth. He...
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Published in: | Proceedings of the National Academy of Sciences - PNAS 2016-08, Vol.113 (33), p.9162-9170 |
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description | Agents that cause Lyme disease, relapsing fever, leptospirosis, and syphilis belong to the phylum Spirochaetae—a unique lineage of bacteria most known for their long, spiral morphology. Despite the relevance to human health, little is known about the most fundamental aspects of spirochete growth. Here, using quantitative microscopy to track peptidoglycan cell-wall synthesis, we found that the Lyme disease spirochete Borrelia burgdorferi displays a complex pattern of growth. B. burgdorferi elongates from discrete zones that are both spatially and temporally regulated. In addition, some peptidoglycan incorporation occurs along the cell body, with the notable exception of a large region at the poles. Newborn cells inherit a highly active zone of peptidoglycan synthesis at midcell that contributes to elongation for most of the cell cycle. Concomitant with the initiation of nucleoid separation and cell constriction, second and third zones of elongation are established at the 1/4 and 3/4 cellular positions, marking future sites of division for the subsequent generation. Positioning of elongation zones along the cell is robust to cell length variations and is relatively precise over long distances (>30 μm), suggesting that cells ‟sense” relative, as opposed to absolute, cell length to establish zones of peptidoglycan synthesis. The transition from one to three zones of peptidoglycan growth during the cell cycle is also observed in relapsing fever Borrelia. However, this mode of growth does not extend to representative species from other spirochetal genera, suggesting that this distinctive growth mode represents an evolutionary divide in the spirochete phylum. |
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Despite the relevance to human health, little is known about the most fundamental aspects of spirochete growth. Here, using quantitative microscopy to track peptidoglycan cell-wall synthesis, we found that the Lyme disease spirochete Borrelia burgdorferi displays a complex pattern of growth. B. burgdorferi elongates from discrete zones that are both spatially and temporally regulated. In addition, some peptidoglycan incorporation occurs along the cell body, with the notable exception of a large region at the poles. Newborn cells inherit a highly active zone of peptidoglycan synthesis at midcell that contributes to elongation for most of the cell cycle. Concomitant with the initiation of nucleoid separation and cell constriction, second and third zones of elongation are established at the 1/4 and 3/4 cellular positions, marking future sites of division for the subsequent generation. Positioning of elongation zones along the cell is robust to cell length variations and is relatively precise over long distances (>30 μm), suggesting that cells ‟sense” relative, as opposed to absolute, cell length to establish zones of peptidoglycan synthesis. The transition from one to three zones of peptidoglycan growth during the cell cycle is also observed in relapsing fever Borrelia. However, this mode of growth does not extend to representative species from other spirochetal genera, suggesting that this distinctive growth mode represents an evolutionary divide in the spirochete phylum.</description><identifier>ISSN: 0027-8424</identifier><identifier>EISSN: 1091-6490</identifier><identifier>DOI: 10.1073/pnas.1610805113</identifier><identifier>PMID: 27506799</identifier><language>eng</language><publisher>United States: National Academy of Sciences</publisher><subject>Bacteria ; Biological Sciences ; Borrelia - growth & development ; Borrelia burgdorferi ; Borrelia burgdorferi - growth & development ; Cell Cycle ; Cells ; Humans ; INAUGURAL ARTICLE ; Leptospira ; Lyme disease ; Lyme Disease - microbiology ; Microscopy ; Peptidoglycan - biosynthesis ; Polymers ; Relapsing Fever - microbiology ; Treponema pallidum</subject><ispartof>Proceedings of the National Academy of Sciences - PNAS, 2016-08, Vol.113 (33), p.9162-9170</ispartof><rights>Volumes 1–89 and 106–113, copyright as a collective work only; author(s) retains copyright to individual articles</rights><rights>Copyright National Academy of Sciences Aug 16, 2016</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c435t-269d51780c87f455f003b73db8dc6c5ce89ce3cb3ce3611176066a7e65c1131c3</citedby><cites>FETCH-LOGICAL-c435t-269d51780c87f455f003b73db8dc6c5ce89ce3cb3ce3611176066a7e65c1131c3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/26471399$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/26471399$$EHTML$$P50$$Gjstor$$H</linktohtml><link.rule.ids>230,314,723,776,780,881,27901,27902,53766,53768,58213,58446</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/27506799$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Jutras, Brandon Lyon</creatorcontrib><creatorcontrib>Scott, Molly</creatorcontrib><creatorcontrib>Parry, Bradley</creatorcontrib><creatorcontrib>Biboy, Jacob</creatorcontrib><creatorcontrib>Gray, Joe</creatorcontrib><creatorcontrib>Vollmer, Waldemar</creatorcontrib><creatorcontrib>Jacobs-Wagner, Christine</creatorcontrib><title>Lyme disease and relapsing fever Borrelia elongate through zones of peptidoglycan synthesis that mark division sites of daughter cells</title><title>Proceedings of the National Academy of Sciences - PNAS</title><addtitle>Proc Natl Acad Sci U S A</addtitle><description>Agents that cause Lyme disease, relapsing fever, leptospirosis, and syphilis belong to the phylum Spirochaetae—a unique lineage of bacteria most known for their long, spiral morphology. 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Positioning of elongation zones along the cell is robust to cell length variations and is relatively precise over long distances (>30 μm), suggesting that cells ‟sense” relative, as opposed to absolute, cell length to establish zones of peptidoglycan synthesis. The transition from one to three zones of peptidoglycan growth during the cell cycle is also observed in relapsing fever Borrelia. 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subjects | Bacteria Biological Sciences Borrelia - growth & development Borrelia burgdorferi Borrelia burgdorferi - growth & development Cell Cycle Cells Humans INAUGURAL ARTICLE Leptospira Lyme disease Lyme Disease - microbiology Microscopy Peptidoglycan - biosynthesis Polymers Relapsing Fever - microbiology Treponema pallidum |
title | Lyme disease and relapsing fever Borrelia elongate through zones of peptidoglycan synthesis that mark division sites of daughter cells |
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