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Chromosome Segregation in Archaea Mediated by a Hybrid DNA Partition Machine

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Chromosome Segregation in Archaea Mediated by a Hybrid DNA Partition Machine Chromosome segregation in Archaea mediated by a hybrid DNA partition machine Anne K. Kalliomaa-Sanforda, Fernando A. Rodriguez-Castañedaa, Brett N. McLeoda, Victor Latorre-Rosellóa, Jasmine H. Smitha, Julia Reimannb, Sonja V. Albersb, and Daniela Barillàa,1 aDepartment of Biology, University of York, Wentworth Way, York YO10 5DD, United Kingdom; and bMax Planck Institute for Terrestrial Microbiology, Karl-von-Frisch-Strasse 10, D-35043 Marburg, Germany Edited by Stanley N. Cohen, Stanford University School of Medicine, Stanford, CA, and approved January 10, 2012 (received for review August 15, 2011) Eukarya and, more recently, some bacteria have been shown to rely actin-like, or tubulin-like (3). Although dissimilar in primary on a cytoskeleton-based apparatus to drive chromosome segrega- sequence and structure, upon nucleotide binding many of these tion. In contrast, the factors and mechanisms underpinning this NTPases polymerize into extensive filaments that move apart the fundamental process are underexplored in archaea, the third do- newly replicated plasmids to opposite cell poles. Walker-type parti- main of life. Here we establish that the archaeon Sulfolobus solfa- tion cassettes are the most widespread. They encode an ATPase, taricus harbors a hybrid segrosome consisting of two interacting ParA, harboring a Walker motif, and a DNA-binding protein, proteins, SegA and SegB, that play a key role in genome segrega- ParB. ParA, specified by several plasmids, assembles into filaments tion in this organism. SegA is an ortholog of bacterial, Walker-type and has been proposed as the dynamic component of a mitotic ParA proteins, whereas SegB is an archaea-specific factor lacking spindle-like apparatus in bacteria (4–7). Segregation cassettes of sequence identity to either eukaryotic or bacterial proteins, but the parAB class are found also on most bacterial chromosomes (8). sharing homology with a cluster of uncharacterized factors con- Mechanistic insights into how ParAB proteins mediate chromo- served in both crenarchaea and euryarchaea, the two major archae- some segregation have been provided by studies on Vibrio cholerae al sub-phyla. We show that SegA is an ATPase that polymerizes in and Caulobacter crescentus. Both exhibit an asymmetric chromo- vitro and that SegB is a site-specific DNA-binding protein contact- some segregation pattern: in newborn cells the origin of replication ing palindromic sequences located upstream of the segAB cassette. is located close to the old pole and, after replication, one of the SegB interacts with SegA in the presence of nucleotides and origins is translocated to the opposite, new pole (9, 10). V. c h o l e r a e dramatically affects its polymerization dynamics. Our data demon- has two chromosomes that replicate and segregate independently. strate that SegB strongly stimulates SegA polymerization, possibly Both contain a Walker-type cassette specifying ParA and ParB by promoting SegA nucleation and accelerating polymer growth. orthologs. Microscopy studies have shown that ParAI encoded by Increased expression levels of segAB resulted in severe growth chromosome I assembles into a comet-like structure that pulls the and chromosome segregation defects, including formation of an- origin of the chromosome from the old to the new cell pole. ParBI ucleate cells, compact nucleoids confined to one half of the cell bound to the centromere site of the chromosome (located in proxi- compartment and fragmented nucleoids. The overall picture emer- mity to the origin of replication) lags behind and is translocated ging from our findings indicates that the SegAB complex fulfills a across the cell by the shrinking ParAI structure (10). Cells in which crucial function in chromosome segregation and is the prototype of parAI is deleted display chromosome I segregation defects. These a DNA partition machine widespread across archaea. observations suggest a model in which the V. c h o l e r a e Par system mediates chromosome I segregation via a mitosis-like pulling me- nucleoid ∣ polymerization ∣ segrosome ∣ Sulfolobus ∣ Walker-type ParA chanism. Similarly, ParA and ParB of C. crescentus are components of a segrosome in which ParA polymerizes into an elongated band very organism, whether unicellular or multicellular, needs to that pulls the chromosome from the old to the new pole (11). Eensure an accurate distribution of its genetic material to the Deletion or overexpression of parA and parB causes filamentous progeny to preserve survival of the species. In both eukaryotic cell morphology and disrupts cell division and chromosome segre- and prokaryotic cells, the machine involved in genome segrega- gation (9). tion includes DNA-anchoring factors and polymeric proteins In contrast with bacteria, our knowledge concerning chromo- capable of driving DNA molecules apart in dividing cells. some segregation in archaea, the third domain of life, is very The events underpinning chromosome segregation in eukar- restricted. The nucleoid undergoes changes in shape and conden- yotes have been extensively investigated. During mitosis, the sation during the cell cycle in the model organism Sulfolobus microtubules of the mitotic spindle capture sister chromatids and solfataricus and a long interval occurs between termination of pull them to opposite spindle poles (1). The mechanisms and key chromosome replication and genome partitioning (12). Newly players behind chromosome segregation in prokaryotes are not replicated chromosomes are held together for a prolonged time yet fully elucidated. However considerable progress has been made during the G2 phase of the cell cycle (13). However, the mole- in deciphering this process in bacteria in the last two decades. An cular mechanisms and factors underpinning chromosome segre- important principle that has emerged is that chromosomes are gation in archaea are terra incognita. actively translocated to specific cellular addresses prior to cell divi- Here we have investigated an uncharacterized segregation lo- sion. The most detailed picture of how a segregation-designed cus harbored by the chromosome of S. solfataricus. The sso0034 apparatus drives DNA molecules to specific cellular locations derives from studies on low copy number plasmids. These mobile Author contributions: A.K.K.-S., F.A.R.-C., B.N.M., and D.B. designed research; A.K.K.-S., elements harbor a dedicated partition cassette consisting of three F.A.R.-C., B.N.M., V.L.-R., J.H.S., and J.R. performed research; J.R. and S.V.A. contributed components: a gene encoding a NTPase, a second gene encoding a new reagents/analytic tools; A.K.K.-S., F.A.R.-C., B.N.M., and D.B. analyzed data; and D.B. DNA-binding protein, and a cis-acting centromere-like site located wrote the paper. in proximity to the genes. The DNA-binding factor directly con- The authors declare no conflict of interest. tacts the centromere and recruits the NTPase. The resulting com- This article is a PNAS Direct Submission. plex drives the attached plasmids to specific subcellular locations 1To whom correspondence should be addressed. E-mail: [email protected]. (2). Partition cassettes belong to three main classes on the basis of This article contains supporting information online at www.pnas.org/lookup/suppl/ the NTPase that they encode, which can be either Walker-type, doi:10.1073/pnas.1113384109/-/DCSupplemental. 3754–3759 ∣ PNAS ∣ March 6, 2012 ∣ vol. 109 ∣ no. 10 www.pnas.org/cgi/doi/10.1073/pnas.1113384109 Downloaded by guest on September 24, 2021 gene specifies an ortholog of bacterial ParA partition proteins SegB is a Dimeric Protein Displaying a α-Helix-Rich Secondary Struc- (14). The 3′ end of sso0034 overlaps the start of a short gene, ture. To investigate the function of SegB, the protein was purified sso0035, encoding a hypothetical protein of unknown function. from E. coli. Dimethyl pimelimidate (DMP) crosslinking experi- We have defined the biochemical function of both proteins and ments clearly showed that SegB forms dimers (Fig. 1A). This re- established that increasing their concentration in the cell results sult was confirmed by size-exclusion chromatography/multiangle in severe defects in growth and chromosome segregation. Our laser light scattering (SEC-MALLS) analysis that detected dimers findings indicate an involvement of the two proteins in genome with a molecular weight of 34 kDa and no higher oligomers partitioning in S. solfataricus and, in view of this function, we have (Fig. 1B). Circular dichroism (CD) spectroscopy revealed that named them SegA (SSO0034) and SegB (SSO0035) for chromo- SegB is highly thermostable up to 90 °C and is mostly α-helical some segregation. with a low percentage of β-sheet and disordered regions (Fig. 1C). Results SegB is a Site-specific DNA-binding Protein: Identification and Fine- SegA is an ATPase Belonging to the ParA Family of Walker-type DNA Mapping of its Binding Site. SegB was likely to be a DNA-binding Partition Proteins. SegA encoded by the chromosome of the ar- protein based on the location of its gene downstream of a parA chaeon S. solfataricus shares substantial sequence identity with gene. The second gene of a DNA segregation cassette typically bacterial ParA proteins involved in genome segregation. These encodes a DNA-binding protein. In bacterial partition cassettes, factors harbor a divergent Walker A ATP-binding motif, whose the centromere-like sites are located upstream or downstream of consensus is KGG-gKt/s (15). SegA is a 220 residue protein ex- the genes and clustered
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