Abstract
Spatial and numerical regulation of flagellar biosynthesis results in different flagellation patterns specific for each bacterial species. Campylobacter jejuni produces amphitrichous (bipolar) flagella to result in a single flagellum at both poles. These flagella confer swimming motility and a distinctive darting motility necessary for infection of humans to cause diarrheal disease and animals to promote commensalism. In addition to flagellation, symmetrical cell division is spatially regulated so that the divisome forms near the cellular midpoint. We have identified an unprecedented system for spatially regulating cell division in C. jejuni composed by FlhG, a regulator of flagellar number in polar flagellates, and components of amphitrichous flagella. Similar to its role in other polarly-flagellated bacteria, we found that FlhG regulates flagellar biosynthesis to limit poles of C. jejuni to one flagellum. Furthermore, we discovered that FlhG negatively influences the ability of FtsZ to initiate cell division. Through analysis of specific flagellar mutants, we discovered that components of the motor and switch complex of amphitrichous flagella are required with FlhG to specifically inhibit division at poles. Without FlhG or specific motor and switch complex proteins, cell division occurs more often at polar regions to form minicells. Our findings suggest a new understanding for the biological requirement of the amphitrichous flagellation pattern in bacteria that extend beyond motility, virulence, and colonization. We propose that amphitrichous bacteria such as Campylobacter species advantageously exploit placement of flagella at both poles to spatially regulate an FlhG-dependent mechanism to inhibit polar cell division, thereby encouraging symmetrical cell division to generate the greatest number of viable offspring. Furthermore, we found that other polarly-flagellated bacteria produce FlhG proteins that influence cell division, suggesting that FlhG and polar flagella may function together in a broad range of bacteria to spatially regulate division.
Highlights
Due to spatial and numerical regulation of flagellar biosynthesis, bacterial species produce distinct patterns of flagellation
Campylobacter jejuni is a leading cause of gastroenteritis in humans and requires amphitrichous flagella to promote infection of hosts. This pattern of flagellation results in a single flagellum at both poles, which is characteristic of many Campylobacter species, but fairly unusual amongst other motile bacteria
We discovered an unprecedented system to spatially regulate cell division that relies on the FlhG ATPase and amphitrichous flagellar biosynthesis
Summary
Due to spatial and numerical regulation of flagellar biosynthesis, bacterial species produce distinct patterns of flagellation. The FlhF and FlhG proteins have been implicated in spatial or numerical control of flagellar biosynthesis in polar flagellates such as Vibrio and Pseudomonas species and Campylobacter jejuni. FlhG, a member of the ParA superfamily of ATPases, is involved in numerical regulation of monotrichous flagellar biosynthesis in Vibrio and Pseudomonas species, presumably by a mechanism that limits flagellar gene expression so that only one flagellum is produced per bacterial cell [1,2]. MinD alleles on plasmids into wild-type C. jejuni 81–176 SmR or C. jejuni 81–176 SmR DflhG for overexpression or complementation was accomplished by amplifying the alleles with primers containing 5’ BamHI restriction sites immediately upstream of the start and stop codons of the respective genes. To increase expression of ftsZ in C. jejuni SmR flhGD61A (MB1054), ftsZ was amplified from chromosomal DNA of C. jejuni 81–176 using primers containing 5’ BamHI restriction sites immediately upstream of the start and stop codons of the gene. Expression of ftsZ from this plasmid, along with constitutive expression of ftsZ from the native chromosomal locus allowed for expression of ftsZ at increased levels relative to wild-type C. jejuni
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