细菌三维基因组学研究
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摘要
作为原核生物,细菌染色体结构的空间组织形式引起了日益广泛的研究兴趣.近年来发展起来的染色体构象捕获和超分辨率显微镜技术,为细菌三维基因组的研究提供了强大的工具.基于染色体构象捕获测序数据,研究人员开发了通用的数据处理流程和染色体三维结构重构软件.目前,已有5个重要的细菌模式物种进行了初步的三维基因组研究,获得了细菌染色体空间组织特征的一些知识,揭示了拟核相关蛋白在细菌三维基因组结构中的重要性,并发现了细菌染色体三维结构与基因转录和细胞周期等过程之间的关联,加深了人们对于细菌三维基因组的认知.本文对近年来细菌三维基因组方面的研究进展进行简要的综述,并指出该领域未来值得关注的一些研究方向.
Bacteria, the most widely distributed species on Earth, play an important role in the biosphere and in human life. Unlike eukaryotes, bacteria do not have a nucleus, and most of the bacterial genetic materials are concentrated in a specific area of the cell, known as the nucleoid. Bacterial cells vary in morphology and are rich in genetic diversity. However, until now,little is known about the way in which bacterial chromosomes are organized. Are the chromosomes in the bacteria randomly distributed or are there specific organization patterns? With the rise of genome sequencing technology, more and more regulatory elements in bacteria have been resolved. The one-dimensional organization pattern of the bacterial genome has gradually become clear. There are several sets of evidence that the genome layout is not random. The chromosome conformation capture and super-resolution microscopy technology developed in recent years provide a powerful tool for the study of bacterial three-dimensional genomes; the former is often a high-throughput method using cell populations as experimental materials, while the latter is low-throughput method based on single-cell molecular markers; these two methods are usually used in conjunction with each other. The sequencing data obtained by 3 C/Hi-C technology can be processed in common pipelines like eukaryotes. In recent years, some software tools for constructing the three-dimensional structures of chromosomes based on 3 C/Hi-C data have appeared, but they are usually aimed at eukaryotic species, and tools for prokaryotes have yet to be developed. At present, five bacterial model species, namely, Caulobacter crescentus,Escherichia coli, Bacillus subtilis, Vibrio cholerae, Mycoplasma pneumoniae, have undergone preliminary threedimensional genome research, and some knowledge about the spatial organization characteristics of bacterial chromosomes has been obtained, revealing the important roles of nucleoid-associated proteins in chromosomal spatial organization. It was found that bacterial chromosomal spatial organization is connected with gene transcription and cell cycles, which has greatly extended our knowledge on the three-dimensional genome of bacteria. However, compared with eukaryotes, the research on the three-dimensional genome of prokaryotes is still insufficient. In view of the complexity of biological processes, the spatial structure of bacterial chromosome is correlated with intracellular and external signal stimulation responses, gene expression regulation, protein interactions, and metabolic processes. Understanding the physiological functions of bacterial three-dimensional genomes from a systematic perspective will be the research focus in future.
Bacteria, the most widely distributed species on Earth, play an important role in the biosphere and in human life. Unlike eukaryotes, bacteria do not have a nucleus, and most of the bacterial genetic materials are concentrated in a specific area of the cell, known as the nucleoid. Bacterial cells vary in morphology and are rich in genetic diversity. However, until now,little is known about the way in which bacterial chromosomes are organized. Are the chromosomes in the bacteria randomly distributed or are there specific organization patterns? With the rise of genome sequencing technology, more and more regulatory elements in bacteria have been resolved. The one-dimensional organization pattern of the bacterial genome has gradually become clear. There are several sets of evidence that the genome layout is not random. The chromosome conformation capture and super-resolution microscopy technology developed in recent years provide a powerful tool for the study of bacterial three-dimensional genomes; the former is often a high-throughput method using cell populations as experimental materials, while the latter is low-throughput method based on single-cell molecular markers; these two methods are usually used in conjunction with each other. The sequencing data obtained by 3 C/Hi-C technology can be processed in common pipelines like eukaryotes. In recent years, some software tools for constructing the three-dimensional structures of chromosomes based on 3 C/Hi-C data have appeared, but they are usually aimed at eukaryotic species, and tools for prokaryotes have yet to be developed. At present, five bacterial model species, namely, Caulobacter crescentus,Escherichia coli, Bacillus subtilis, Vibrio cholerae, Mycoplasma pneumoniae, have undergone preliminary threedimensional genome research, and some knowledge about the spatial organization characteristics of bacterial chromosomes has been obtained, revealing the important roles of nucleoid-associated proteins in chromosomal spatial organization. It was found that bacterial chromosomal spatial organization is connected with gene transcription and cell cycles, which has greatly extended our knowledge on the three-dimensional genome of bacteria. However, compared with eukaryotes, the research on the three-dimensional genome of prokaryotes is still insufficient. In view of the complexity of biological processes, the spatial structure of bacterial chromosome is correlated with intracellular and external signal stimulation responses, gene expression regulation, protein interactions, and metabolic processes. Understanding the physiological functions of bacterial three-dimensional genomes from a systematic perspective will be the research focus in future.
引文
1 Nemergut D R,Costello E K,Hamady M,et al.Global patterns in the biogeography of bacterial taxa.Environ MicroBiol,2011,13:135-144
2 Sezonov G,Joseleau-Petit D,D’Ari R.Escherichia coli physiology in luria-bertani broth.J Bacteriol,2007,189:8746-8749
3 Jacob F,Monod J.Genetic regulatory mechanisms in the synthesis of proteins.J Mol Biol,1961,3:318-356
4 Huynen M A,Snel B.Gene and context:Integrative approaches to genome analysis.Adv Protein Chem,2000,54:345-379
5 Junier I,Hérisson J,Képès F.Genomic organization of evolutionarily correlated genes in bacteria:Limits and strategies.J Mol Biol,2012,419:369-386
6 Wright M A,Kharchenko P,Church G M,et al.Chromosomal periodicity of evolutionarily conserved gene pairs.Proc Natl Acad Sci USA,2007,104:10559-10564
7 Képès F.Periodic transcriptional organization of the E.coli,genome.J Mol Biol,2004,340:957-964
8 Jeong K S,Ahn J,Khodursky A B.Spatial patterns of transcriptional activity in the chromosome of Escherichia coli.Genome Biol,2004,5:R86
9 Weng X,Xiao J.Spatial organization of transcription in bacterial cells.Trends Genets,2014,30:287-297
10 Cook P R.A model for all genomes:The role of transcription factories.J Mol Biol,2010,395:1-10
11 Dekker J,Rippe K,Dekker M,et al.Capturing chromosome conformation.Science,2002,295:1306-1311
12 Simonis M,Klous P,Splinter E,et al.Nuclear organization of active and inactive chromatin domains uncovered by chromosome conformation capture-on-chip(4C).Nat Genet,2006,38:1348-1354
13 Zhao Z,Tavoosidana G,Sj?linder M,et al.Circular chromosome conformation capture(4C)uncovers extensive networks of epigenetically regulated intra-and interchromosomal interactions.Nat Genet,2006,38:1341-1347
14 Dostie J,Richmond T A,Arnaout R A,et al.Chromosome conformation capture carbon copy(5C):A massively parallel solution for mapping interactions between genomic elements.Genome Res,2006,16:1299-1309
15 Lieberman-Aiden E,van Berkum N L,Williams L,et al.Comprehensive mapping of long-range interactions reveals folding principles of the human genome.Science,2009,326:289-293
16 Fullwood M J,Liu M H,Pan Y F,et al.An oestrogen-receptor-α-bound human chromatin interactome.Nature,2009,462:58-64
17 Bonev B,Cavalli G.Organization and function of the 3D genome.Nat Rev Genet,2016,17:661-678
18 Sydor A M,Czymmek K J,Puchner E M,et al.Super-resolution microscopy:From single molecules to supramolecular assemblies.Trends Cell Biol,2015,25:730-748
19 Stracy M,Uphoff S,Garza de Leon F,et al.In vivo single-molecule imaging of bacterial DNA replication,transcription,and repair.FEBS Lett,2014,588:3585-3594
20 Krogh T J,M?ller-Jensen J,Kaleta C.Impact of chromosomal architecture on the function and evolution of bacterial genomes.Front Microbiol,2018,9:2019
21 Le T B K,Imakaev M V,Mirny L A,et al.High-resolution mapping of the spatial organization of a bacterial chromosome.Science,2013,342:731-734
22 Umbarger M A,Toro E,Wright M A,et al.The three-dimensional architecture of a bacterial genome and its alteration by genetic perturbation.Mol Cell,2011,44:252-264
23 Lioy V S,Cournac A,Marbouty M,et al.Multiscale structuring of the E.coli chromosome by nucleoid-associated and condensin proteins.Cell,2018,172:771-783.e18
24 Cagliero C,Grand R S,Jones M B,et al.Genome conformation capture reveals that the Escherichia coli chromosome is organized by replication and transcription.Nucleic Acids Res,2013,41:6058-6071
25 Marbouty M,Le Gall A,Cattoni D I,et al.Condensin-and replication-mediated bacterial chromosome folding and origin condensation revealed by Hi-C and super-resolution imaging.Mol Cell,2015,59:588-602
26 Wang X,Brand?o H B,Le T B K,et al.Bacillus subtilis SMC complexes juxtapose chromosome arms as they travel from origin to terminus.Science,2017,355:524-527
27 Wang X,Le T B K,Lajoie B R,et al.Condensin promotes the juxtaposition of DNA flanking its loading site in Bacillus subtilis.Genes Dev,2015,29:1661-1675
28 Val M E,Marbouty M,de Lemos Martins F,et al.A checkpoint control orchestrates the replication of the two chromosomes of Vibrio cholerae.Sci Adv,2016,2:e1501914
29 Trussart M,Yus E,Martinez S,et al.Defined chromosome structure in the genome-reduced bacterium Mycoplasma pneumoniae.Nat Commun,2017,8:14665
30 Lewis P J,Thaker S D,Errington J.Compartmentalization of transcription and translation in Bacillus subtilis.EMBO J,2000,19:710-718
31 Robinow C,Kellenberger E.The bacterial nucleoid revisited.Microbiol Rev,1994,58:211-232
32 Wang W,Li G W,Chen C,et al.Chromosome organization by a nucleoid-associated protein in live bacteria.Science,2011,333:1445-1449
33 Huang B,Bates M,Zhuang X.Super-resolution fluorescence microscopy.Annu Rev Biochem,2009,78:993-1016
34 Gavrilov A A,Gushchanskaya E S,Strelkova O,et al.Disclosure of a structural milieu for the proximity ligation reveals the elusive nature of an active chromatin hub.Nucleic Acids Res,2013,41:3563-3575
35 Louwers M,Splinter E,van Driel R,et al.Studying physical chromatin interactions in plants using chromosome conformation capture(3C).Nat Protoc,2009,4:1216-1229
36 Belton J M,McCord R P,Gibcus J H,et al.Hi-C:A comprehensive technique to capture the conformation of genomes.Methods,2012,58:268-276
37 Lin D,Hong P,Zhang S,et al.Digestion-ligation-only Hi-C is an efficient and cost-effective method for chromosome conformation capture.Nat Genet,2018,50:754-763
38 Li H,Durbin R.Fast and accurate short read alignment with burrows-wheeler transform.Bioinformatics,2009,25:1754-1760
39 Langmead B,Trapnell C,Pop M,et al.Ultrafast and memory-efficient alignment of short DNA sequences to the human genome.Genome Biol,2009,10:R25
40 Yaffe E,Tanay A.Probabilistic modeling of Hi-C contact maps eliminates systematic biases to characterize global chromosomal architecture.Nat Genet,2011,43:1059-1065
41 Hu M,Deng K,Selvaraj S,et al.Hicnorm:Removing biases in Hi-C data via poisson regression.Bioinformatics,2012,28:3131-3133
42 Cournac A,Marie-Nelly H,Marbouty M,et al.Normalization of a chromosomal contact map.BMC Genomics,2012,13:436
43 Imakaev M,Fudenberg G,McCord R P,et al.Iterative correction of Hi-C data reveals hallmarks of chromosome organization.Nat Methods,2012,9:999-1003
44 Servant N,Varoquaux N,Lajoie B R,et al.Hic-pro:An optimized and flexible pipeline for Hi-C data processing.Genome Biol,2015,16:259
45 Wingett S W,Ewels P,Furlan-Magaril M,et al.Hicup:Pipeline for mapping and processing Hi-C data.F1000 Res,2015,4:1310
46 Heinz S,Benner C,Spann N,et al.Simple combinations of lineage-determining transcription factors prime cis-regulatory elements required for macrophage and b cell identities.Mol Cell,2010,38:576-589
47 Durand N C,Shamim M S,Machol I,et al.Juicer provides a one-click system for analyzing loop-resolution Hi-C experiments.Cell Syst,2016,3:95-98
48 Serra F,Di Stefano M,Spill Y G,et al.Restraint-based three-dimensional modeling of genomes and genomic domains.FEBS Lett,2015,589:2987-2995
49 Lajoie B R,Dekker J,Kaplan N.The Hitchhiker’s guide to Hi-C analysis:Practical guidelines.Methods,2015,72:65-75
50 Peng C,Fu L Y,Dong P F,et al.The sequencing bias relaxed characteristics of Hi-C derived data and implications for chromatin 3D modeling.Nucleic Acids Res,2013,41:e183
51 Zhang Z Z,Li G,Toh K C,et al.3D chromosome modeling with semi-definite programming and Hi-C data.J Comput Biol,2013,20:831-846
52 Serra F,BaùD,Goodstadt M,et al.Automatic analysis and 3D-modelling of Hi-C data using tadbit reveals structural features of the fly chromatin colors.PLoS Comput Biol,2017,13:e1005665
53 Rieber L,Mahony S.Minimds:3D structural inference from high-resolution Hi-C data.Bioinformatics,2017,33:i261-i266
54 Oluwadare O,Cheng J.Clustertad:An unsupervised machine learning approach to detecting topologically associated domains of chromosomes from Hi-C data.BMC BioInf,2017,18:480
55 Kabsch W.A solution for the best rotation to relate two sets of vectors.Acta Cryst A,1976,32:922-923
56 Lesne A,Riposo J,Roger P,et al.3D genome reconstruction from chromosomal contacts.Nat Methods,2014,11:1141-1143
57 Trieu T,Cheng J.Mogen:A tool for reconstructing 3D models of genomes from chromosomal conformation capturing data.Bioinformatics,2016,32:1286-1292
58 Hu M,Deng K,Qin Z,et al.Bayesian inference of spatial organizations of chromosomes.PLoS Comput Biol,2013,9:e1002893
59 Varoquaux N,Ay F,Noble W S,et al.A statistical approach for inferring the 3D structure of the genome.Bioinformatics,2014,30:i26-i33
60 Adhikari B,Trieu T,Cheng J.Chromosome 3D:Reconstructing three-dimensional chromosomal structures from Hi-C interaction frequency data using distance geometry simulated annealing.BMC Genomics,2016,17:886
61 Hacker W C,Li S,Elcock A H.Features of genomic organization in a nucleotide-resolution molecular model of the Escherichia coli chromosome.Nucleic Acids Res,2017,45:7541-7554
62 Goodsell D S,Autin L,Olson A J.Lattice models of bacterial nucleoids.J Phys Chem B,2018,122:5441-5447
63 Yildirim A,Feig M.High-resolution 3D models of caulobacter crescentus chromosome reveal genome structural variability and organization.Nucleic Acids Res,2018,46:3937-3952
64 Dillon S C,Dorman C J.Bacterial nucleoid-associated protein,nucleoid structure and gene expression.Nat Rev Microbiol,2010,8:185-195
65 Gruber S.SMC complexes sweeping through the chromosome:Going with the flow and against the tide.Curr Opin MicroBiol,2018,42:96-103
66 Hirano T.Condensin-based chromosome organization from bacteria to vertebrates.Cell,2016,164:847-857
67 Wang X,Hughes A C,Brand?o H B,et al.In vivo evidence for atpase-dependent dna translocation by the Bacillus subtilis SMC condensin complex.Mol Cell,2018,71:841-847.e5
68 Le T B,Laub M T.Transcription rate and transcript length drive formation of chromosomal interaction domain boundaries.EMBO J,2016,35:1582-1595
2 Sezonov G,Joseleau-Petit D,D’Ari R.Escherichia coli physiology in luria-bertani broth.J Bacteriol,2007,189:8746-8749
3 Jacob F,Monod J.Genetic regulatory mechanisms in the synthesis of proteins.J Mol Biol,1961,3:318-356
4 Huynen M A,Snel B.Gene and context:Integrative approaches to genome analysis.Adv Protein Chem,2000,54:345-379
5 Junier I,Hérisson J,Képès F.Genomic organization of evolutionarily correlated genes in bacteria:Limits and strategies.J Mol Biol,2012,419:369-386
6 Wright M A,Kharchenko P,Church G M,et al.Chromosomal periodicity of evolutionarily conserved gene pairs.Proc Natl Acad Sci USA,2007,104:10559-10564
7 Képès F.Periodic transcriptional organization of the E.coli,genome.J Mol Biol,2004,340:957-964
8 Jeong K S,Ahn J,Khodursky A B.Spatial patterns of transcriptional activity in the chromosome of Escherichia coli.Genome Biol,2004,5:R86
9 Weng X,Xiao J.Spatial organization of transcription in bacterial cells.Trends Genets,2014,30:287-297
10 Cook P R.A model for all genomes:The role of transcription factories.J Mol Biol,2010,395:1-10
11 Dekker J,Rippe K,Dekker M,et al.Capturing chromosome conformation.Science,2002,295:1306-1311
12 Simonis M,Klous P,Splinter E,et al.Nuclear organization of active and inactive chromatin domains uncovered by chromosome conformation capture-on-chip(4C).Nat Genet,2006,38:1348-1354
13 Zhao Z,Tavoosidana G,Sj?linder M,et al.Circular chromosome conformation capture(4C)uncovers extensive networks of epigenetically regulated intra-and interchromosomal interactions.Nat Genet,2006,38:1341-1347
14 Dostie J,Richmond T A,Arnaout R A,et al.Chromosome conformation capture carbon copy(5C):A massively parallel solution for mapping interactions between genomic elements.Genome Res,2006,16:1299-1309
15 Lieberman-Aiden E,van Berkum N L,Williams L,et al.Comprehensive mapping of long-range interactions reveals folding principles of the human genome.Science,2009,326:289-293
16 Fullwood M J,Liu M H,Pan Y F,et al.An oestrogen-receptor-α-bound human chromatin interactome.Nature,2009,462:58-64
17 Bonev B,Cavalli G.Organization and function of the 3D genome.Nat Rev Genet,2016,17:661-678
18 Sydor A M,Czymmek K J,Puchner E M,et al.Super-resolution microscopy:From single molecules to supramolecular assemblies.Trends Cell Biol,2015,25:730-748
19 Stracy M,Uphoff S,Garza de Leon F,et al.In vivo single-molecule imaging of bacterial DNA replication,transcription,and repair.FEBS Lett,2014,588:3585-3594
20 Krogh T J,M?ller-Jensen J,Kaleta C.Impact of chromosomal architecture on the function and evolution of bacterial genomes.Front Microbiol,2018,9:2019
21 Le T B K,Imakaev M V,Mirny L A,et al.High-resolution mapping of the spatial organization of a bacterial chromosome.Science,2013,342:731-734
22 Umbarger M A,Toro E,Wright M A,et al.The three-dimensional architecture of a bacterial genome and its alteration by genetic perturbation.Mol Cell,2011,44:252-264
23 Lioy V S,Cournac A,Marbouty M,et al.Multiscale structuring of the E.coli chromosome by nucleoid-associated and condensin proteins.Cell,2018,172:771-783.e18
24 Cagliero C,Grand R S,Jones M B,et al.Genome conformation capture reveals that the Escherichia coli chromosome is organized by replication and transcription.Nucleic Acids Res,2013,41:6058-6071
25 Marbouty M,Le Gall A,Cattoni D I,et al.Condensin-and replication-mediated bacterial chromosome folding and origin condensation revealed by Hi-C and super-resolution imaging.Mol Cell,2015,59:588-602
26 Wang X,Brand?o H B,Le T B K,et al.Bacillus subtilis SMC complexes juxtapose chromosome arms as they travel from origin to terminus.Science,2017,355:524-527
27 Wang X,Le T B K,Lajoie B R,et al.Condensin promotes the juxtaposition of DNA flanking its loading site in Bacillus subtilis.Genes Dev,2015,29:1661-1675
28 Val M E,Marbouty M,de Lemos Martins F,et al.A checkpoint control orchestrates the replication of the two chromosomes of Vibrio cholerae.Sci Adv,2016,2:e1501914
29 Trussart M,Yus E,Martinez S,et al.Defined chromosome structure in the genome-reduced bacterium Mycoplasma pneumoniae.Nat Commun,2017,8:14665
30 Lewis P J,Thaker S D,Errington J.Compartmentalization of transcription and translation in Bacillus subtilis.EMBO J,2000,19:710-718
31 Robinow C,Kellenberger E.The bacterial nucleoid revisited.Microbiol Rev,1994,58:211-232
32 Wang W,Li G W,Chen C,et al.Chromosome organization by a nucleoid-associated protein in live bacteria.Science,2011,333:1445-1449
33 Huang B,Bates M,Zhuang X.Super-resolution fluorescence microscopy.Annu Rev Biochem,2009,78:993-1016
34 Gavrilov A A,Gushchanskaya E S,Strelkova O,et al.Disclosure of a structural milieu for the proximity ligation reveals the elusive nature of an active chromatin hub.Nucleic Acids Res,2013,41:3563-3575
35 Louwers M,Splinter E,van Driel R,et al.Studying physical chromatin interactions in plants using chromosome conformation capture(3C).Nat Protoc,2009,4:1216-1229
36 Belton J M,McCord R P,Gibcus J H,et al.Hi-C:A comprehensive technique to capture the conformation of genomes.Methods,2012,58:268-276
37 Lin D,Hong P,Zhang S,et al.Digestion-ligation-only Hi-C is an efficient and cost-effective method for chromosome conformation capture.Nat Genet,2018,50:754-763
38 Li H,Durbin R.Fast and accurate short read alignment with burrows-wheeler transform.Bioinformatics,2009,25:1754-1760
39 Langmead B,Trapnell C,Pop M,et al.Ultrafast and memory-efficient alignment of short DNA sequences to the human genome.Genome Biol,2009,10:R25
40 Yaffe E,Tanay A.Probabilistic modeling of Hi-C contact maps eliminates systematic biases to characterize global chromosomal architecture.Nat Genet,2011,43:1059-1065
41 Hu M,Deng K,Selvaraj S,et al.Hicnorm:Removing biases in Hi-C data via poisson regression.Bioinformatics,2012,28:3131-3133
42 Cournac A,Marie-Nelly H,Marbouty M,et al.Normalization of a chromosomal contact map.BMC Genomics,2012,13:436
43 Imakaev M,Fudenberg G,McCord R P,et al.Iterative correction of Hi-C data reveals hallmarks of chromosome organization.Nat Methods,2012,9:999-1003
44 Servant N,Varoquaux N,Lajoie B R,et al.Hic-pro:An optimized and flexible pipeline for Hi-C data processing.Genome Biol,2015,16:259
45 Wingett S W,Ewels P,Furlan-Magaril M,et al.Hicup:Pipeline for mapping and processing Hi-C data.F1000 Res,2015,4:1310
46 Heinz S,Benner C,Spann N,et al.Simple combinations of lineage-determining transcription factors prime cis-regulatory elements required for macrophage and b cell identities.Mol Cell,2010,38:576-589
47 Durand N C,Shamim M S,Machol I,et al.Juicer provides a one-click system for analyzing loop-resolution Hi-C experiments.Cell Syst,2016,3:95-98
48 Serra F,Di Stefano M,Spill Y G,et al.Restraint-based three-dimensional modeling of genomes and genomic domains.FEBS Lett,2015,589:2987-2995
49 Lajoie B R,Dekker J,Kaplan N.The Hitchhiker’s guide to Hi-C analysis:Practical guidelines.Methods,2015,72:65-75
50 Peng C,Fu L Y,Dong P F,et al.The sequencing bias relaxed characteristics of Hi-C derived data and implications for chromatin 3D modeling.Nucleic Acids Res,2013,41:e183
51 Zhang Z Z,Li G,Toh K C,et al.3D chromosome modeling with semi-definite programming and Hi-C data.J Comput Biol,2013,20:831-846
52 Serra F,BaùD,Goodstadt M,et al.Automatic analysis and 3D-modelling of Hi-C data using tadbit reveals structural features of the fly chromatin colors.PLoS Comput Biol,2017,13:e1005665
53 Rieber L,Mahony S.Minimds:3D structural inference from high-resolution Hi-C data.Bioinformatics,2017,33:i261-i266
54 Oluwadare O,Cheng J.Clustertad:An unsupervised machine learning approach to detecting topologically associated domains of chromosomes from Hi-C data.BMC BioInf,2017,18:480
55 Kabsch W.A solution for the best rotation to relate two sets of vectors.Acta Cryst A,1976,32:922-923
56 Lesne A,Riposo J,Roger P,et al.3D genome reconstruction from chromosomal contacts.Nat Methods,2014,11:1141-1143
57 Trieu T,Cheng J.Mogen:A tool for reconstructing 3D models of genomes from chromosomal conformation capturing data.Bioinformatics,2016,32:1286-1292
58 Hu M,Deng K,Qin Z,et al.Bayesian inference of spatial organizations of chromosomes.PLoS Comput Biol,2013,9:e1002893
59 Varoquaux N,Ay F,Noble W S,et al.A statistical approach for inferring the 3D structure of the genome.Bioinformatics,2014,30:i26-i33
60 Adhikari B,Trieu T,Cheng J.Chromosome 3D:Reconstructing three-dimensional chromosomal structures from Hi-C interaction frequency data using distance geometry simulated annealing.BMC Genomics,2016,17:886
61 Hacker W C,Li S,Elcock A H.Features of genomic organization in a nucleotide-resolution molecular model of the Escherichia coli chromosome.Nucleic Acids Res,2017,45:7541-7554
62 Goodsell D S,Autin L,Olson A J.Lattice models of bacterial nucleoids.J Phys Chem B,2018,122:5441-5447
63 Yildirim A,Feig M.High-resolution 3D models of caulobacter crescentus chromosome reveal genome structural variability and organization.Nucleic Acids Res,2018,46:3937-3952
64 Dillon S C,Dorman C J.Bacterial nucleoid-associated protein,nucleoid structure and gene expression.Nat Rev Microbiol,2010,8:185-195
65 Gruber S.SMC complexes sweeping through the chromosome:Going with the flow and against the tide.Curr Opin MicroBiol,2018,42:96-103
66 Hirano T.Condensin-based chromosome organization from bacteria to vertebrates.Cell,2016,164:847-857
67 Wang X,Hughes A C,Brand?o H B,et al.In vivo evidence for atpase-dependent dna translocation by the Bacillus subtilis SMC condensin complex.Mol Cell,2018,71:841-847.e5
68 Le T B,Laub M T.Transcription rate and transcript length drive formation of chromosomal interaction domain boundaries.EMBO J,2016,35:1582-1595