Secondary chromosome

Chromids,[1] formerly (and less specifically) secondary chromosomes,[lower-alpha 1] are a class of bacterial replicons (replicating DNA molecules). These replicons are called "chromids" because they have characteristic features of both chromosomes and plasmids. Early on, it was thought that all core genes could be found on the main chromosome of the bacteria. However, in 1989 a replicon (now known as a chromid) was discovered containing core genes outside of the main chromosome. These core genes make the chromid indispensable to the organism. Chromids are large replicons, although not as large as the main chromosome. However, chromids are almost always larger than a plasmid (or megaplasmid). Chromids also share many genomic signatures of the chromosome, including their GC-content and their codon usage bias. On the other hand, chromids do not share the replication systems of chromosomes. Instead, they use the replication system of plasmids. Chromids are present in 10% of bacteria species sequenced by 2009.[5]

Bacterial genomes divided between a main chromosome and one or more chromids (and / or megaplasmids) are said to be divided or multipartite genomes. The vast majority of chromid-encoding bacteria only have a single chromid, although 9% have more than one (compared with 12% of megaplasmid-encoding bacteria containing multiple megaplasmids). The genus Azospirillum contains three species which have up to five chromids, the most chromids known in a single species to date. Chromids also appear to be more common in bacteria which have a symbiotic or pathogenic relationship with eukaryotes[6] and with organisms with high tolerance to abiotic stressors.[7]

Chromids were discovered in 1989, in a species of Alphaproteobacteria known as Rhodobacter sphaeroides.[8] However, the formalization of the concept of a "chromid" as an independent type of replicon only came about in 2010.[1] Several classifications further distinguish between chromids depending on conditions of their essentiality, their replication system, and more.

The two hypotheses for the origins of chromids are the "plasmid" and "schism" hypotheses. According to the plasmid hypothesis, chromids originate from plasmids which have acquired core genes over evolutionary time and so stabilized in their respective lineages. According to the schism hypothesis, chromids as well as the main chromosome originate from a schism of a larger, earlier chromosome. The plasmid hypothesis is presently widely accepted, although there may be rare cases where large replicons originate from a chromosomal schism. One finding holds that chromids originated 45 times across bacterial phylogenies and were lost twice.[6]

Discovery and classification

Discovery

Early in the era of bacterial genomics, the genomes of bacteria were thought to have a relatively simple architecture. All known bacteria had circular chromosomes containing all the crucial genes. Some bacteria had additional replicons known as plasmids, and plasmids were characteristically small, circular, and dispensable (meaning that they only encoded non-essential genes).[9] As more bacteria and their genomes were studied, many alternative forms of bacterial genomic architecture began to be discovered. Linear chromosomes and linear plasmids were discovered in a number of species. Soon after, bacteria with several large replicons were discovered, leading to the view that bacteria, just like eukaryotes, can have a genome made up of more than one chromosome.[9] The first example of this was Rhodobacter sphaeroides in 1989,[8] but additional discoveries quickly followed with Brucella melitensis in 1993,[10] Burkholderia cepacia complex in 1994,[11] Rhizobium meliloti in 1995,[12] Bacillus thuringiensis in 1996,[13] and now about 10% of bacterial species are known to have large replicons that are separate from the main chromosome.

Definition

With the onset of these discoveries, several approaches in classifying different components of multipartite genomes were proposed. Various terms have been used to describe large replicons other than the main chromosome, including simply designating them as additional chromosomes, or "minichromosomes", "megaplasmids", or "secondary chromosomes". Criteria used to distinguish between these replicons typically revolve around features such as size and the presence of core genes.[9] In 2010, the classification of these genomic elements as chromids was proposed. Previous terms, such as "secondary chromosome", are considered inadequate upon the observation that these replicons contain the replication systems of plasmids and so are a fundamentally different class of replicons than chromosomes.[14] The original definition of a 'chromid' involves meeting three criteria:[5]

  1. chromids have plasmid-type maintenance and replication systems;
  2. chromids have a nucleotide composition close to that of the chromosome;
  3. chromids carry core genes that are found on the chromosome in other species.

While this definition is robust, the authors who proposed it did so with the expectation that some exceptions would be found that would blur the lines between chromids and other replicons. This expectation existed because of the general tendency for evolutionary lineages to produce ambiguous systems, which has resulted in the more well-known issues in formulating a widely-encompassing species definition.[5]

Since the classification of chromids, other replicons have been discovered which share some features of chromids but have been categorized separately. One example is the designated "rrn-plasmid" found in a clade within the bacterial genus Aureimonas. The rrn-plasmid contains the rrn (rRNA) operon (hence its name), and the rrn operon cannot be found on the main chromosome. The main chromosome is therefore termed as an "rrn-lacking chromosome" or RLC, and so the clade of bacteria within Aureimonas which possess the rrn-plasmid is also termed the "RLC clade". Members of the RLC clade have nine replicons, of which the main chromosome is the largest and the rrn-plasmid is the smallest at only 9.4kb. The rrn-plasmid also has a high copy number in RLC bacteria. While this very small size and copy number resembles plasmids moreso than it does chromids, the rrn-plasmid still ahs the only copies of the genes in the rrn operon and for tRNA(Ile). This distinctive collection of features led the scientists discovering this replicon to simply classify it as an rrn-plasmid, which is thought of as a separate classification than a "plasmid" or "chromid".[15]

Additional proposed classifications

Beyond classifying certain replicons as chromids, a number of scientists have proposed further distinguishing between different types of chromids. One classification distinguishes between primary and secondary chromids. Primary chromids are defined as chromids containing core genes that are always essential for the survival of the bacterium under all conditions. Secondary chromids are defined as chromids essential for survival in the native conditions of the bacterium, but may be non-essential in certain "safe" conditions such as a laboratory environment. Secondary chromids may also have more recent evolutionary origins and may retain some more plasmid-like features as compared with primary chromids. An example of a proposed primary chromid is "chromosome II" of Paracoccus denitrificans PD1222.[6][14]

Characteristics

Size and copy number

In a bacterial genome, the main chromosome will always be the largest replicon, followed by the chromid and then the plasmid. One exception to this trend is known in Deinococcus deserti VCD115, where both plasmids are larger than the chromid.[5]

Chromids vary considerably in size between organisms. In the bacterial genus Vibrio, the main chromosome varies between 3.0–3.3 Mb whereas the chromid varies between 0.8–2.4 Mb in size.[16] A replicon in a strain of Buchnera, which encodes some core genes, is only 7.8kb.[17] While the presence of core genes may lead to the classification of this replicon as a chromid, this replicon may also be excluded on certain definitions. Some approaches only categorize certain replicons as chromids if they meet a threshold size of 350kb. It has also been observed that chromids tend to have a low copy number in the cell, as with chromosomes and megaplasmids. On average, chromids are twice as large as megaplasmids (and so the emergence of a chromid from a megaplasmid is associated with a sizable gene accumulation in the aftermath of the conversion).[6] One of the largest chromids is the one in Burkholderia pseudomallei, which exceeds 3.1 million nucleotides in size, i.e. 3.1 megabases or 3.1 Mb.[18]

Genomic features

Chromids more frequently have a lower G + C content compared with the main chromosome, although the strength of this association is not very strong. A chromid will also typically have a G + C content within 1% of that of the main chromosome, reflecting its nearing the base composition equilibrium of the main chromosome after having stably existed within a bacterial lineage for a necessary period of time. Chromids also resemble the main chromosome in their codon usage bias.[5][19] One analysis found that chromids had a median 0.34% difference in GC content with the main chromosome, compared with values of 1.9% for megaplasmids and 2.8% for plasmids.[6]

Chromids have at least one core gene absent from the main chromosome. (Main chromosomes contain the bulk of the core genes of a bacterium, whereas plasmids contain no core genes.) For example, the chromid in Vibrio cholerae contains genes for the ribosomal subunits L20 and L35.[20] While most chromids have a disproportionately smaller number of essential genes compared to the main chromosome, such as rRNA genes or the genes in the rRNA operon, some may have many more essential genes and may even be considered "equal partners" with the chromosome.[21] In general, chromids also see an enrichment of genes involved in the processes of transport, metabolism, transcription, regulatory functions, signal transduction, and motility-related functions. Proteins located on chromids are involved in processes which can interact with proteins encoded on the main chromosome. Chromids also have more transposase genes than chromosomes, but less than megaplasmids.[6]

Phylogenetic distribution

The presence of core genes makes the chromid essential to the survival of the bacterium. The same core genes will be found on the chromids within a genus but not necessarily between genera. All chromids of a genus may additionally share a large number of conserved but non-essential genes which help define the phenotype of the genus (and the emergence of chromids appears to be the primary evolutionary force in the formation of chromid-encoding bacterial genera, as has been suggested in the case of Vibrio[19]). In contrast, bacterial chromosomes may universally or near-universally share hundreds of conserved core genes. Plasmids contain no core genes, and unlike chromids, plasmids of different species within a bacterial genus (or even just different isolates within the same species) share few genes. This is partly due to the common transfer of gain and loss of plasmids and their transfer between bacteria through conjugation (a form of horizontal gene transfer), while chromids are passed on through cell divisions (vertically) with no evidence of chromids moving through horizontal gene transfer.[5] It has been observed that the chromid in at least one bacterial species could be eliminated without making the bacterium inviable, however, the bacterium did become auxotrophic indicating a severe fitness compromise associated with the loss of the chromid.[22]

Due to their stable presence within a bacterial genus, chromids also have a feature of being phylogenetically restricted to specific genera. Examples of genera of bacteria with chromids include Deinococcus, Leptospira, Cyanothece (a type of cyanobacteria), and an enrichment of genera of the Pseudomonadota. Overall, bacterial genome sequencing indicates that roughly 10% of bacterial species have a chromid.[5] It has also been found that there is a bias towards co-occurrence of a chromid and a megaplasmid in the same organism. Chromids also appear more frequently in phylogenies than do megaplasmids (in approximately twice as many species), despite megaplasmids being the putative evolutionary source for chromids. This may result in the tendency of organisms to lose their megaplasmids over time, compared with the inherently greater evolutionary stability of chromids.[6]

Replication

Chromids share features of the replication of both chromosomes and chromids. For one, chromids use the replication system of plasmids. While plasmids do not replicate in coordination with the main chromosome or the cell cycle,[23] chromids do and only replicate once per cell cycle.[24] In the bacterial genus Vibrio, replication of the main chromosome begins before replication of the chromid. The chromid is smaller than the chromosome, and so takes a shorter amount of time to finish replication. For this reason, replication of the chromid is delayed to coordinate replication termination between the chromosome and chromid.[25] Earlier replication of the chromosome compared with the chromid has also been observed in Ensifer meliloti.[26] Bacteria also rely on different replication factors to start replication between the chromosome and the chromid.[27] Replication of the chromosome is initiated upon stimulation of the expression of the protein DnaA, whereas expression of chromid replication requires DnaA but also depends on RctB. This is similar to F1 and P plasmids which also depend on DnaA but still have their replication controlled by other proteins (specifically RepA and RepE).[28] Segregation of the chromid follows different patterns between different genera of bacteria, although it typically takes place after the segregation of the main chromosome.[6]

So far, chromids are known to replicate with one of two types of systems: either with the repABC system or with iterons.[1]

Evolutionary flexibility

Several studies indicate that chromids are less conserved and evolve more rapidly than do chromosomes in bacteria. In a study of many species of the genus Vibrio, it was found that the main, large chromosome had a consistent size range of 3–3.3 Mb, whereas the secondary chromosome flexibly ranged from 0.8–2.4 Mb. This considerable variation indicates a greater degree of structural flexibility. Bacteria of the genus Agrobacterium and another genera can have three or more chromids, and these multiple chromids in several strains commonly undergo large-scale rearrangements which can involve the translocation of one sizable portion of one chromid into another.[16] Genes located on chromids are also more prone to evolve and display less purifying selection. Since common species definition for prokaryotes are based on DNA sequence or average nucleotide identity, the greater evolvability of the chromid may result in organisms with chromids having a greater tendency to speciate.[29]

Origins

"Schism" and "plasmid" hypotheses

Several suggestions have been put forwards to explain the origins of chromids. The two main hypotheses are the "schism hypothesis" and the "plasmid hypothesis". According to the schism hypothesis, two separate bacterial chromosomes may arise through the splitting of one larger chromosome, resulting in a main and a secondary chromosome (or a chromid). However, due to the plasmid-type maintenance and replication systems in chromids as well as the uneven distribution of core genes between the main chromosome and the chromid, the plasmid hypothesis suggesting that chromids evolved from megaplasmids which acquired core genes is widely accepted.[19] Once megaplasmids acquire core genes from the main chromosome, combined with the simultaneous loss of those core genes from the main chromosome, the plasmid becomes a stable and required element of the bacterial genome. (Megaplasmids may also acquire duplicate copies of core genes from the main chromosome. The existence of the duplicate core gene may degenerate on the main chromosome, leading to its sole presence on the newly formed chromid. In this case, the chromid is formed through a neutral transition.) This event also stabilizes the other genes located on the new chromid, which may result in a characteristic phenotype for the new lineage. These core genes can transfer to a megaplasmid through several means. One is homologous recombination between the main chromosome and the plasmid. It is also possible that an existing chromid could recombine with a plasmid to gain its replication system. Once a chromid appears in a lineage, it is stable over long evolutionary periods. Several bacteria genera have chromids which are characteristic to each genus. Whereas the chromids found in a single genus may universally share a large number of genes, there are no genes universally found across the chromids of different genera.[5]

Plasmids are almost always if not always the source for the origins of chromids, but at least two bacterial strains may have their large replicons derive from the schism of a larger chromosome. In these exceptional cases, the term "secondary chromosome" may be retained to describe them and so, in this sense, differentiate them from "chromids". Identifying a replicon as a "secondary chromosome" may be done on the basis of conserved synteny and random distribution of core genes with the main chromosome.[6]

Proposed adaptive causes

The question of the origins of chromids is tied to the question of why they evolved. One possibility is that chromids are a "frozen accident", where they simply happened to evolve by chance and for no particular reason and so, for this reason alone, are present in the lineage descendant from the organism in which they emerged. In this scenario, core genes end up on the chromid by chance, but the chance fixation of core genes on the secondary replicon through neutral transitions leads to its essentiality to the organism. However, chromids may also bring some advantages which helps the bacterium compete in its environment. It has been observed that bacteria with chromids are capable of growing faster in culture, and also contain fairly more sizable genomes. Chromid-encoding bacteria have a genome with an average size of 5.73 ± 1.66 Mb, whereas bacteria which do not encode chromids have an average genome size of 3.38 ± 1.81 Mb. For this reason, some have concluded that the placement of a number of genes on the chromid instead of the main chromosome allows for genome expansion without compromising replication speed and efficiency.[5] On the other hand, two thirds of bacterial genomes over 6 Mb are not multipartite and only three of the fifty largest genomes are multipartite, and so a larger genome has not yet been causally demonstrated as a reason for the evolutionary origins of a chromid. Chromids can also be frequently found on fast-growing bacteria, suggesting their contribution to replication and division speed, although here too several analyses have raised difficulties with this suggestion as a driving evolutionary force for the emergence of chromids. Instead, it is more likely that genome expansion and faster replication speed may be involved in the maintenance of chromids in lineages but not a causal explanation for their emergence.[6] Chromids may also allow for coordinated expression of niche-specific genes.[30][31] Random though rare emergence of chromids which happen to have the necessary genes to confer an advantageous lifestyle in a given environment may play an important role in stabilizing that chromid in the organism and leading to a new lineage defined by the presence of the now crucial replicon.[32]

References

  1. ↑ Some secondary chromosomes are not chromids. For example, the secondary chromosome of Brucella melitensis carries no plasmid-like replication systems and instead use the standard DnaA/oriC,[2] even though its relatives in Ochrobactrum use a RepABC system.[3] The chromid mode of replicon generation is also only seen in bacteria (as of 2023) and archaeal "secondary chromosomes" replicate like normal chromosomes.[4]
  1. 1 2 3 Fournes, Florian; Val, Marie-Eve; Skovgaard, Ole; Mazel, Didier (2018). "Replicate Once Per Cell Cycle: Replication Control of Secondary Chromosomes". Frontiers in Microbiology. 9: 1833. doi:10.3389/fmicb.2018.01833. ISSN 1664-302X. PMC 6090056. PMID 30131796.
  2. ↑ DelVecchio, VG; Kapatral, V; Redkar, RJ; Patra, G; Mujer, C; Los, T; Ivanova, N; Anderson, I; Bhattacharyya, A; Lykidis, A; Reznik, G; Jablonski, L; Larsen, N; D'Souza, M; Bernal, A; Mazur, M; Goltsman, E; Selkov, E; Elzer, PH; Hagius, S; O'Callaghan, D; Letesson, JJ; Haselkorn, R; Kyrpides, N; Overbeek, R (8 January 2002). "The genome sequence of the facultative intracellular pathogen Brucella melitensis". Proceedings of the National Academy of Sciences of the United States of America. 99 (1): 443–8. Bibcode:2002PNAS...99..443D. doi:10.1073/pnas.221575398. PMC 117579. PMID 11756688.
  3. ↑ Krzyżanowska, DM; Maciąg, T; Ossowicki, A; Rajewska, M; Kaczyński, Z; Czerwicka, M; Rąbalski, Ł; Czaplewska, P; Jafra, S (2019). "Ochrobactrum quorumnocens sp. nov., a quorum quenching bacterium from the potato rhizosphere, and comparative genome analysis with related type strains". PLOS ONE. 14 (1): e0210874. doi:10.1371/journal.pone.0210874. PMC 6342446. PMID 30668584.
  4. ↑ Ausiannikava, D; Mitchell, L; Marriott, H; Smith, V; Hawkins, M; Makarova, KS; Koonin, EV; Nieduszynski, CA; Allers, T (1 August 2018). "Evolution of Genome Architecture in Archaea: Spontaneous Generation of a New Chromosome in Haloferax volcanii". Molecular Biology and Evolution. 35 (8): 1855–1868. doi:10.1093/molbev/msy075. PMC 6063281. PMID 29668953.
  5. 1 2 3 4 5 6 7 8 9 Harrison, Peter W.; Lower, Ryan P.J.; Kim, Nayoung K.D.; Young, J. Peter W. (2010). "Introducing the bacterial 'chromid': not a chromosome, not a plasmid". Trends in Microbiology. 18 (4): 141–148. doi:10.1016/j.tim.2009.12.010. PMID 20080407.
  6. 1 2 3 4 5 6 7 8 9 10 diCenzo, George C.; Finan, Turlough M. (2017-08-09). "The Divided Bacterial Genome: Structure, Function, and Evolution". Microbiology and Molecular Biology Reviews. 81 (3). doi:10.1128/MMBR.00019-17. PMC 5584315. PMID 28794225.
  7. ↑ Sonnenberg, Cecilie Bækkedal; Haugen, Peik (2021-09-01). "The Pseudoalteromonas multipartite genome: distribution and expression of pangene categories, and a hypothesis for the origin and evolution of the chromid". G3: Genes, Genomes, Genetics. 11 (9): jkab256. doi:10.1093/g3journal/jkab256. ISSN 2160-1836. PMC 8496264. PMID 34544144.
  8. 1 2 Suwanto, A; Kaplan, S (1989). "Physical and genetic mapping of the Rhodobacter sphaeroides 2.4.1 genome: presence of two unique circular chromosomes". Journal of Bacteriology. 171 (11): 5850–5859. doi:10.1128/jb.171.11.5850-5859.1989. ISSN 0021-9193. PMC 210445. PMID 2808300.
  9. 1 2 3 Ochman, Howard (2002-06-25). "Bacterial Evolution: Chromosome Arithmetic and Geometry". Current Biology. 12 (12): R427–R428. doi:10.1016/S0960-9822(02)00916-8. ISSN 0960-9822. PMID 12123594. S2CID 7121998.
  10. ↑ Michaux, S; Paillisson, J; Carles-Nurit, M J; Bourg, G; Allardet-Servent, A; Ramuz, M (1993). "Presence of two independent chromosomes in the Brucella melitensis 16M genome". Journal of Bacteriology. 175 (3): 701–705. doi:10.1128/jb.175.3.701-705.1993. ISSN 0021-9193. PMC 196208. PMID 8423146.
  11. ↑ Cheng, H P; Lessie, T G (1994). "Multiple replicons constituting the genome of Pseudomonas cepacia 17616". Journal of Bacteriology. 176 (13): 4034–4042. doi:10.1128/jb.176.13.4034-4042.1994. ISSN 0021-9193. PMC 205602. PMID 7517389.
  12. ↑ Honeycutt, R. J.; McClelland, M.; Sobral, B. W. (1993). "Physical map of the genome of Rhizobium meliloti 1021". Journal of Bacteriology. 175 (21): 6945–6952. doi:10.1128/jb.175.21.6945-6952.1993. PMC 206821. PMID 8226638.
  13. ↑ Carlson, Cathrine Rein; Johansen, Trine; Lecadet, Marguerite-M.; Kolsto, Anne-BritYR 1996 (1996). "Genomic organization of the entomopathogenic bacterium Bacillus thuringiensis subsp. berliner 1715". Microbiology. 142 (7): 1625–1634. doi:10.1099/13500872-142-7-1625. ISSN 1465-2080.
  14. 1 2 Dziewit, Lukasz; Czarnecki, Jakub; Wibberg, Daniel; Radlinska, Monika; Mrozek, Paulina; Szymczak, Michal; Schlüter, Andreas; Pühler, Alfred; Bartosik, Dariusz (2014). "Architecture and functions of a multipartite genome of the methylotrophic bacterium Paracoccus aminophilus JCM 7686, containing primary and secondary chromids". BMC Genomics. 15 (1): 124. doi:10.1186/1471-2164-15-124. ISSN 1471-2164. PMC 3925955. PMID 24517536.
  15. ↑ Anda, Mizue; Ohtsubo, Yoshiyuki; Okubo, Takashi; Sugawara, Masayuki; Nagata, Yuji; Tsuda, Masataka; Minamisawa, Kiwamu; Mitsui, Hisayuki (2015-11-17). "Bacterial clade with the ribosomal RNA operon on a small plasmid rather than the chromosome". Proceedings of the National Academy of Sciences. 112 (46): 14343–14347. Bibcode:2015PNAS..11214343A. doi:10.1073/pnas.1514326112. ISSN 0027-8424. PMC 4655564. PMID 26534993.
  16. 1 2 Okada, Kazuhisa; Iida, Tetsuya; Kita-Tsukamoto, Kumiko; Honda, Takeshi (2005-01-15). "Vibrios Commonly Possess Two Chromosomes". Journal of Bacteriology. 187 (2): 752–757. doi:10.1128/JB.187.2.752-757.2005. ISSN 0021-9193. PMC 543535. PMID 15629946.
  17. ↑ Shigenobu, Shuji; Watanabe, Hidemi; Hattori, Masahira; Sakaki, Yoshiyuki; Ishikawa, Hajime (2000). "Genome sequence of the endocellular bacterial symbiont of aphids Buchnera sp. APS". Nature. 407 (6800): 81–86. Bibcode:2000Natur.407...81S. doi:10.1038/35024074. ISSN 1476-4687. PMID 10993077. S2CID 4405072.
  18. ↑ Holden, M. T. G.; Titball, R. W.; Peacock, S. J.; Cerdeno-Tarraga, A. M.; Atkins, T.; Crossman, L. C.; Pitt, T.; Churcher, C.; Mungall, K.; Bentley, S. D.; Sebaihia, M. (2004-09-28). "Genomic plasticity of the causative agent of melioidosis, Burkholderia pseudomallei". Proceedings of the National Academy of Sciences. 101 (39): 14240–14245. doi:10.1073/pnas.0403302101. ISSN 0027-8424. PMC 521101. PMID 15377794.
  19. 1 2 3 Egan, Elizabeth S.; Fogel, Michael A.; Waldor, Matthew K. (2005-03-30). "Divided genomes: negotiating the cell cycle in prokaryotes with multiple chromosomes: Multiple chromosomes in prokaryotes". Molecular Microbiology. 56 (5): 1129–1138. doi:10.1111/j.1365-2958.2005.04622.x. PMID 15882408. S2CID 12362731.
  20. ↑ Waldor, Matthew K.; RayChaudhuri, Debabrata (2000-08-03). "Treasure trove for cholera research". Nature. 406 (6795): 469–470. doi:10.1038/35020178. ISSN 0028-0836. PMID 10952295. S2CID 205007987.
  21. ↑ Mackenzie, Chris; Choudhary, Madhusudan; Larimer, Frank W.; Predki, Paul F.; Stilwagen, Stephanie; Armitage, Judith P.; Barber, Robert D.; Donohue, Timothy J.; Hosler, Jonathan P.; Newman, Jack E.; Shapleigh, James P. (2001). "The home stretch, a first analysis of the nearly completed genome of Rhodobacter sphaeroides 2.4.1". Photosynthesis Research. 70 (1): 19–41. doi:10.1023/A:1013831823701. PMID 16228360. S2CID 1035709.
  22. ↑ Hynes, Michael F.; Quandt, Jürgen; O'Connell, Michael P.; Pühler, Alfred (1989). "Direct selection for curing and deletion of Rhizobium plasmids using transposons carrying the Bacillus subtilis sacB gene". Gene. 78 (1): 111–120. doi:10.1016/0378-1119(89)90319-3. PMID 2548927.
  23. ↑ del Solar, Gloria; Giraldo, Rafael; Ruiz-Echevarría, María Jesús; Espinosa, Manuel; Díaz-Orejas, Ramón (1998). "Replication and Control of Circular Bacterial Plasmids". Microbiology and Molecular Biology Reviews. 62 (2): 434–464. doi:10.1128/MMBR.62.2.434-464.1998. ISSN 1092-2172. PMC 98921. PMID 9618448.
  24. ↑ Egan, Elizabeth S; Løbner-Olesen, Anders; Waldor, Matthew K (2004). "Synchronous replication initiation of the two Vibrio cholerae chromosomes". Current Biology. 14 (13): R501–R502. doi:10.1016/j.cub.2004.06.036. PMID 15242627. S2CID 6532702.
  25. ↑ Rasmussen, Tue; Bugge Jensen, Rasmus; Skovgaard, Ole (2007-07-11). "The two chromosomes of Vibrio cholerae are initiated at different time points in the cell cycle". The EMBO Journal. 26 (13): 3124–3131. doi:10.1038/sj.emboj.7601747. ISSN 0261-4189. PMC 1914095. PMID 17557077.
  26. ↑ Nisco, Nicole J. De; Abo, Ryan P.; Wu, C. Max; Penterman, Jon; Walker, Graham C. (2014-03-04). "Global analysis of cell cycle gene expression of the legume symbiont Sinorhizobium meliloti". Proceedings of the National Academy of Sciences. 111 (9): 3217–3224. Bibcode:2014PNAS..111.3217D. doi:10.1073/pnas.1400421111. ISSN 0027-8424. PMC 3948222. PMID 24501121.
  27. ↑ Egan, Elizabeth S.; Waldor, Matthew K. (2003-08-22). "Distinct Replication Requirements for the Two Vibrio cholerae Chromosomes". Cell. 114 (4): 521–530. doi:10.1016/S0092-8674(03)00611-1. ISSN 0092-8674. PMID 12941279. S2CID 17177569.
  28. ↑ Duigou, Stéphane; Knudsen, Kristine G.; Skovgaard, Ole; Egan, Elizabeth S.; Løbner-Olesen, Anders; Waldor, Matthew K. (2006). "Independent Control of Replication Initiation of the Two Vibrio cholerae Chromosomes by DnaA and RctB". Journal of Bacteriology. 188 (17): 6419–6424. doi:10.1128/JB.00565-06. PMC 1595377. PMID 16923911.
  29. ↑ Cooper, Vaughn S.; Vohr, Samuel H.; Wrocklage, Sarah C.; Hatcher, Philip J. (2010-04-01). Wilke, Claus O. (ed.). "Why Genes Evolve Faster on Secondary Chromosomes in Bacteria". PLOS Computational Biology. 6 (4): e1000732. Bibcode:2010PLSCB...6E0732C. doi:10.1371/journal.pcbi.1000732. ISSN 1553-7358. PMC 2848543. PMID 20369015.
  30. ↑ Heidelberg, John F.; Eisen, Jonathan A.; Nelson, William C.; Clayton, Rebecca A.; Gwinn, Michelle L.; Dodson, Robert J.; Haft, Daniel H.; Hickey, Erin K.; Peterson, Jeremy D.; Umayam, Lowell; Gill, Steven R. (2000-08-03). "DNA sequence of both chromosomes of the cholera pathogen Vibrio cholerae". Nature. 406 (6795): 477–483. Bibcode:2000Natur.406..477H. doi:10.1038/35020000. ISSN 0028-0836. PMC 8288016. PMID 10952301.
  31. ↑ Okada, Kazuhisa; Iida, Tetsuya; Kita-Tsukamoto, Kumiko; Honda, Takeshi (2005-01-15). "Vibrios Commonly Possess Two Chromosomes". Journal of Bacteriology. 187 (2): 752–757. doi:10.1128/JB.187.2.752-757.2005. ISSN 0021-9193. PMC 543535. PMID 15629946.
  32. ↑ Chain, Patrick S. G.; Denef, Vincent J.; Konstantinidis, Konstantinos T.; Vergez, Lisa M.; Agulló, Loreine; Reyes, Valeria Latorre; Hauser, Loren; Córdova, Macarena; Gómez, Luis; González, Myriam; Land, Miriam (2006-10-17). "Burkholderia xenovorans LB400 harbors a multi-replicon, 9.73-Mbp genome shaped for versatility". Proceedings of the National Academy of Sciences. 103 (42): 15280–15287. doi:10.1073/pnas.0606924103. ISSN 0027-8424. PMC 1622818. PMID 17030797.
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