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International Journal of Evolutionary Biology logoLink to International Journal of Evolutionary Biology
. 2011 Jan 24;2011:685015. doi: 10.4061/2011/685015

Distribution of Genes Encoding Nucleoid-Associated Protein Homologs in Plasmids

Toshiharu Takeda 1, Choong-Soo Yun 1, 2,2, Masaki Shintani 3, Hisakazu Yamane 1, Hideaki Nojiri 1, 2,2,*
PMCID: PMC3042613  PMID: 21350637

Abstract

Bacterial nucleoid-associated proteins (NAPs) form nucleoprotein complexes and influence the expression of genes. Recent studies have shown that some plasmids carry genes encoding NAP homologs, which play important roles in transcriptional regulation networks between plasmids and host chromosomes. In this study, we determined the distributions of the well-known NAPs Fis, H-NS, HU, IHF, and Lrp and the newly found NAPs MvaT and NdpA among the whole-sequenced 1382 plasmids found in Gram-negative bacteria. Comparisons between NAP distributions and plasmid features (size, G+C content, and putative transferability) were also performed. We found that larger plasmids frequently have NAP gene homologs. Plasmids with H-NS gene homologs had less G+C content. It should be noted that plasmids with the NAP gene homolog also carried the relaxase gene involved in the conjugative transfer of plasmids more frequently than did those without the NAP gene homolog, implying that plasmid-encoded NAP homologs positively contribute to transmissible plasmids.

1. Introduction

Bacterial chromosomal DNA is folded to form a compacted structure, the nucleoid. The proteins involved in folding the chromosome are known as nucleoid-associated proteins (NAPs) [1, 2]. Because of their DNA-binding ability, NAPs can also play an important role in global gene regulation [1, 2]. Each well-known NAP in Enterobacteriaceae may be categorized as a “factor for inversion stimulation” (Fis), “histone-like nucleoid structuring protein” (H-NS), “histone-like protein from Escherichia coli strain U93” (HU), “integration host factor” (IHF), or “leucine-responsive regulatory protein” (Lrp) [1]. Fis is one of the most abundant NAPs in exponentially growing E. coli cells, and its role as a transcriptional regulator has been investigated [3]. H-NS binds DNA, especially A+T-rich regions including promoter regions or horizontally acquired DNA and acts as a global transcriptional repressor [4]. HU and IHF are similar in amino acid sequence level, and both are global regulators [5, 6], although they have distinct DNA-binding activities: HU binds to DNA nonspecifically whereas IHF binds to a consensus sequence [7]. Lrp has a global influence on transcription regulation and is also involved in microbial virulence [8]. In addition to these well-known NAPs, many other NAPs are found not only in Enterobacteriaceae but also in other organisms. For instance, NdpA, a functionally unknown NAP, has been found in Gram-negative bacteria [9]. The MvaT family protein is the functional homolog of H-NS in Pseudomonas bacteria [10].

Horizontal gene transfer (HGT), which is mediated by transduction, transformation, and conjugation, plays an important role in the evolution of prokaryotic genomes [11, 12]. Genes acquired by HGT can provide beneficial functions such as resistance to antibiotics and advantages to their host under selective pressures [13]. However, the mechanisms underlying the integration of newly acquired genes into host regulatory networks are still unclear. Recent investigations have shown that some plasmids carry the genes encoding NAP homologs, which play important roles in transcriptional regulation networks between plasmids and host chromosomes and in maintaining host cell fitness. For example, Doyle et al. [14] reported that plasmid-encoded H-NS-like protein has a “stealth” function that allows for plasmid transfer into host cells without disrupting host regulatory networks, maintaining host cell fitness. Yun and Suzuki et al. [15] reported that plasmid-encoded H-NS-like protein can also play a key role in optimizing gene transcription both on the plasmid and in the host chromosome.

In this study, we determined the distributions of NAP homologs among plasmids and discussed their roles in the maintenance of plasmid and host cell fitness.

2. Materials and Methods

2.1. Plasmid Database Collection and Local BLAST Analyses

The completely sequenced plasmid database was downloaded from the NCBI ftp site (ftp://ftp.ncbi.nih.gov/genomes/Plasmids/). Some duplicated sequence data of the same plasmids were removed from the database. Identification of plasmids that contain the genes encoding NAP homologs was performed using the local TBLASTN program (ver. 2.2.24, ftp://ftp.ncbi.nlm.nih.gov/blast/executables/blast+/LATEST/) under strict conditions (i.e., thresholds of 30% identity and 70% query coverage). The complete amino acid sequences of Fis (DDBJ/EMBL/GenBank accession no. AP_003801), H-NS (AP_001863), Hha (AP_001109), HUα (AP_003818), HUβ (AP_001090), IHFα (AP_002332), IHFβ (AP_001542), Lrp (AP_001519), and NdpA (P33920) from E. coli K-12 W3110 and MvaT (AAP33788) from Pseudomonas aeruginosa PAO1 were used as query sequences.

2.2. Bacterial Genome Analyses

The complete genome sequences of bacteria were downloaded from the NCBI ftp site (ftp://ftp.ncbi.nih.gov/genomes/Bacteria/). The number of NAP genes on proteobacterial genomes was investigated using the TBLASTN program (http://www.ncbi.nlm.nih.gov/sutils/genom_table.cgi) under strict conditions (i.e., thresholds of 30% identity and 70% query coverage).

2.3. Plasmid Classification

Plasmids in the database were classified into six groups according to their source organisms: Gram-negative, Gram-positive, archaeal, eukaryotic, viral, and unclassified. Putative transferability of each Gram-negative plasmid was determined by whether it carried the relaxase gene of each MOB family that Garcillán-Barcia et al. proposed [16]. Instead of using the local PSI-BLAST program (ver. 2.2.24, ftp://ftp.ncbi.nlm.nih.gov/blast/executables/blast+/LATEST/) as described by Garcillán-Barcia et al. [16], we used the local TBLASTN program.

3. Results and Discussion

3.1. Database Collection and Plasmid Classification by Origin

We downloaded the whole sequences of 2278 plasmids from the NCBI ftp site (April 2010). Duplicated plasmids were removed manually, and the resultant 2260 plasmid sequences were used in this study. To understand what types of plasmids were included in the database, we classified them into six groups according to their source organisms. The database included 1382 Gram-negative, 725 Gram-positive, 81 archaeal, 43 eukaryotic, 1 viral, and 28 unclassified plasmids.

3.2. Identification of the Plasmids Containing NAP Gene Homologs

Using the amino acid sequences of well-known NAPs (Fis, H-NS, HU, IHF, and Lrp) and newly found NAPs (MvaT and NdpA), their distributions were surveyed for plasmids using the TBLASTN program. Some plasmids had ORFs showing sequence similarities to both HU and IHF. We adopted the one with the higher E value. Of 2260 plasmids, 155 (7%) contained the gene encoding NAP homolog. Of those, 116 (75%) contained only one NAP gene homolog and 39 (25%) contained more than one NAP gene homolog. No plasmids carried the Fis gene homolog. Twenty-two plasmids carried the H-NS gene homolog, and all of them had a Gram-negative origin (Table 1). Sixty-six plasmids had the HU gene homolog; of these, 51 had a Gram-negative origin and 15 had a Gram-positive origin (Table 2). Twenty-seven plasmids (25 with Gram-negative and 2 with Gram-positive origins) carried the IHF gene homolog (Table 3). Forty-eight plasmids (46 with Gram-negative, 1 with a Gram-positive, and 1 with an archaeal origin) carried the Lrp gene homolog (Table 4). Of these, 23 (48%) contained more than one Lrp gene homolog. On the other hand, MvaT and NdpA homologs were encoded on only 3 plasmids, and all of them were of Gram-negative origin (Table 5). Previously reported plasmids that are known to have NAP gene homologs were included in those 155 plasmids. These included R27 (NC_002305) and pHCM1 (NC_003384) [18, 19] with the H-NS gene homolog; pQBR103 (NC_009444) [20] with the HU and NdpA gene homologs; and pCAR1 (NC_004444) [21, 22] with the MvaT, HU, and NdpA gene homologs. These results indicated the adequacy of our search. Because we used NAPs from Gram-negative bacteria as query sequences, it may be reasonable that 136 (88%) of 155 plasmids with the NAP gene homolog belonged to the group isolated from Gram-negative bacteria. Therefore, in further studies we discussed the Gram-negative plasmid group.

Table 1.

Plasmids containing the gene encoding H-NS homologa.

Plasmid name Accession no. Source organism Length (nt) G+C content (%)b Identity (%)c Query coverage (%) Subject start Subject end Classificationd MOB familye
1 NC_013972 Erwinia amylovora ATCC 49946 28243 50 66 99 3129 2728 −
pAsa5 NC_009350 Aeromonas salmonicida subsp. salmonicida A449 155098 54 46 99 941 534 − MOBF
47 99 16890 16483
pAsal5 NC_009352 Aeromonas salmonicida subsp. salmonicida 18536 54 46 99 12285 12692 −
pEA29 NC_013957 Erwinia amylovora CFBP1430 28259 50 66 99 3129 2728 −
pEA29 NC_005706 Erwinia amylovora 28185 50 64 99 2991 2590 −
pEC-IMP NC_012555 Enterobacter cloacae 318782 48 64 99 109370 108969 − MOBH
pEC-IMPQ NC_012556 Enterobacter cloacae 324503 48 64 99 109370 108969 − MOBH
pEJ30 NC_004834 Erwinia sp. Ejp 556 29593 50 66 99 4651 4250 −
pEP36 NC_013263 Erwinia pyrifoliae Ep1/96 35909 50 66 99 25040 25441 −
pEP36 NC_004445 Erwinia pyrifoliae Ep1/96 35904 50 64 98 4675 4280 −
pET45 NC_010699 Erwinia tasmaniensis Et1/99 44694 51 52 93 37435 37809 − MOBF
pET49 NC_010697 Erwinia tasmaniensis Et1/99 48751 44 36 94 30821 31204 −
pHCM1 NC_003384 Salmonella enterica subsp. enterica serovar Typhi str. CT18 218160 48 61 99 131861 131460 − MOBH
pK2044 NC_006625 Klebsiella pneumoniae NTUH-K2044 224152 50 67 99 35717 36112 −
plasmid_153kb NC_009705 Yersinia pseudotuberculosis IP 31758 153140 40 44 100 139846 140265 −
pLVPK NC_005249 Klebsiella pneumoniae 219385 50 67 99 114397 114792 −
pMAK1 NC_009981 Salmonella enterica subsp. enterica serovar Choleraesuis 208409 47 61 99 60046 59645 − MOBH
pO111_1 NC_013365 Escherichia coli O111:H- str. 11128 204604 47 61 99 80175 79774 − MOBH
pSG1 NC_007713 Sodalis glossinidius str. “morsitans” 83306 49 43 97 2533 2922 −
R27 NC_002305 Salmonella enterica subsp. enterica serovar Typhi 180461 46 61 99 148225 148626 − MOBH
R478 NC_005211 Serratia marcescens 274762 46 64 99 111747 111346 − MOBH
Unnamed NC_011148 Salmonella enterica subsp. enterica serovar Agona str. SL483 37978 41 43 95 7671 7288 −
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aThis list is the result of a TBLASTN analysis using the amino acid sequence of H-NS as a query under strict conditions (i.e., thresholds of 30% identity and 70% query coverage). Besides these plasmids, pSf-R27 from Shigella flexneri 2a str. 2457T was completely sequenced by Wei et al. [17] and encodes the H-NS-like protein Sfh.

bAverage G+C content of the plasmid.

cReported TBLASTN identity to H-NS.

dPlasmid classification according to its source organism (−, Gram-negative plasmid).

ePlasmid classification according to its relaxase gene sequence as described by Garcillán-Barcia et al. [16].

Table 2.

Plasmids containing the gene encoding HU homologa.

Plasmid name Accession no. Source organism Length (nt) G+C content (%)b Identity (%)c Query coverage (%) Subject start Subject end Classificationd MOB familye
1 NC_006823 Aromatoleum aromaticum EbN1 207355 58 55 99 186175 185909 −
1 NC_007949 Polaromonas sp. JS666 360405 57 52 99 61052 60786 − MOBH
1 NC_008010 Deinococcus geothermalis DSM 11300 574127 66 38 97 550805 550545 +
1 NC_008503 Lactococcus lactis subsp. cremoris SK11 14041 34 37 94 9732 10007 + MOBP
1 NC_008242 Chelativorans sp. BNC1 343931 62 41 94 133932 133678 − MOBQ
2 NC_012529 Deinococcus deserti VCD115 314317 64 38 93 269648 269899 +
3 NC_012528 Deinococcus deserti VCD115 396459 61 40 96 8700 8957 +
Megaplasmid NC_007974 Cupriavidus metallidurans CH34 2580084 64 51 99 1393415 1393149 − MOBV
Megaplasmid NC_005863 Desulfovibrio vulgaris str. Hildenborough 202301 66 31 98 5502 5765 −
Megaplasmid pDF308 NC_013940 Deferribacter desulfuricans SSM1 308544 24 41 100 253817 253548 −
Megaplasmid pHG1 NC_005241 Ralstonia eutropha H16 452156 62 48 99 343060 342791 −
p49879.1 NC_006907 Leptospirillum ferrooxidans 28878 58 47 99 3281 3015 − MOBQ
p49879.2 NC_006909 Leptospirillum ferrooxidans 28012 55 48 99 15858 15592 − MOBQ
pAH187_270 NC_011655 Bacillus cereus AH187 270082 34 59 100 113139 112870 +
pAH820_272 NC_011777 Bacillus cereus AH820 272145 34 58 100 153060 152791 +
pAM04528 NC_012693 Salmonella enterica 158213 52 57 99 14067 14333 − MOBH
pAOVO01 NC_008765 Acidovorax sp. JS42 72689 62 46 100 65140 64871 − MOBF
pAPA01-011 NC_013210 Acetobacter pasteurianus IFO 3283-01 191799 53 47 100 154736 154467 −
46 99 38442 38708
pAR060302 NC_012692 Escherichia coli 166530 53 57 99 15755 16021 − MOBH
pAsa4 NC_009349 Aeromonas salmonicida subsp. salmonicida A449 166749 53 60 99 26844 26578 − MOBH
pAtS4c NC_011984 Agrobacterium vitis S4 211620 59 45 94 141245 140991 − MOBQ
pAtS4e NC_011981 Agrobacterium vitis S4 631775 57 41 94 40476 40222 − MOBQ
pBc239 NC_011973 Bacillus cereus Q1 239246 33 52 100 191895 192164 +
pBF9343 NC_006873 Bacteroides fragilis NCTC 9343 36560 32 35 92 15803 15558 − MOBP
pBPHY01 NC_010625 Burkholderia phymatum STM815 1904893 62 43 99 826527 826252 −
pBPHY02 NC_010627 Burkholderia phymatum STM815 595108 59 45 99 98625 98359 −
pBtoxis NC_010076 Bacillus thuringiensis serovar israelensis 127923 32 52 99 77382 77648 +
pBWB401 NC_010180 Bacillus weihenstephanensis KBAB4 417054 34 59 100 338347 338078 +
pCAR1 NC_004444 Pseudomonas resinovorans 199035 56 42 99 97809 98075 − MOBH
pCAUL01 NC_010335 Caulobacter sp. K31 233649 67 44 99 97598 97329 − MOBQ
pCER270 NC_010924 Bacillus cereus 270082 34 59 100 169548 169279 +
pDBORO NC_009137 Lactococcus lactis subsp. lactis bv. diacetylactis 16404 35 37 94 16387 16112 +
pDVUL01 NC_008741 Desulfovibrio vulgaris DP4 198504 66 31 98 198317 198054 −
peH4H NC_012690 Escherichia coli 148105 53 57 99 14067 14333 − MOBH
pG9842_209 NC_011775 Bacillus cereus G9842 209488 30 60 100 88828 88559 +
pH308197_258 NC_011339 Bacillus cereus H3081.97 258484 34 59 100 83033 83302 +
pHD5AT NC_012752 Candidatus Hamiltonella defensa 5AT (Acyrthosiphon pisum) 59032 45 45 99 14981 15247 − MOBP
pIP1202 NC_009141 Yersinia pestis bv. Orientalis str. IP275 182913 53 57 99 14067 14333 − MOBH
plasmid 2 NC_007972 Cupriavidus metallidurans CH34 171459 61 46 99 125530 125261 −
pMOL28 NC_006525 Cupriavidus metallidurans CH34 171461 61 46 99 51529 51798 −
pMP118 NC_007930 Lactobacillus salivarius UCC118 242436 32 54 99 56763 56497 + MOBV
pNPUN02 NC_010632 Nostoc punctiforme PCC 73102 254918 41 44 99 74804 74538 − MOBV
pOANT02 NC_009670 Ochrobactrum anthropi ATCC 49188 101491 59 49 94 32700 32446 −
pP91278 NC_008613 Photobacterium damselae subsp. piscicida 131520 52 57 99 125918 126184 − MOBH
pP99-018 NC_008612 Photobacterium damselae subsp. piscicida 150157 51 57 99 133314 133580 − MOBH
pPER272 NC_010921 Bacillus cereus 272145 34 58 100 153060 152791 +
pPMA4326A NC_005918 Pseudomonas syringae pv. maculicola 46697 55 42 99 1520 1786 −
pPMA4326B NC_005919 Pseudomonas syringae pv. maculicola 40110 55 45 99 1457 1723 −
pQBR103 NC_009444 Pseudomonas fluorescens SBW25 425094 53 51 99 182862 183128 −
pR132503 NC_012853 Rhizobium leguminosarum bv. trifolii WSM1325 516088 59 47 94 300662 300916 − MOBQ
pRA1 NC_012885 Aeromonas hydrophila 143963 51 58 99 15573 15839 − MOBH
pRALTA NC_010529 Cupriavidus taiwanensis 557200 60 46 98 153542 153276 −
pREB1 NC_009926 Acaryochloris marina MBIC11017 374161 47 46 100 339743 340012 − MOBF
pREB2 NC_009927 Acaryochloris marina MBIC11017 356087 45 48 100 57583 57852 − MOBF
pREB3 NC_009928 Acaryochloris marina MBIC11017 273121 45 46 100 234682 234951 − MOBF
42 100 243339 243608
pRL7 NC_008382 Rhizobium leguminosarum bv. viciae 3841 151564 58 48 94 20484 20230 − MOBQ
pRLG203 NC_011370 Rhizobium leguminosarum bv. trifolii WSM2304 308747 58 49 94 141121 140867 −
pRp12D01 NC_012855 Ralstonia pickettii 12D 389779 58 37 99 321346 321080 − MOBH
pSG2 NC_007184 Sodalis glossinidius 27240 45 45 86 10072 9845 −
pSG3 NC_007186 Sodalis glossinidius 19201 51 51 100 13812 13543 −
pSN254 NC_009140 Salmonella enterica subsp. enterica serovar Newport str. SL254 176473 53 57 99 14067 14333 − MOBH
pTiS4 NC_011982 Agrobacterium vitis S4 258824 57 41 94 27356 27102 − MOBQ
40 94 83408 83154
pTi-SAKURA NC_002147 Agrobacterium tumefaciens 206479 56 44 94 95763 95509 − MOBQ
pVSAL840 NC_011311 Aliivibrio salmonicida LFI1238 83540 40 60 99 31361 31627 − MOBF
58 99 77350 77084
pYR1 NC_009139 Yersinia ruckeri 158038 51 57 99 15070 15336 − MOBH
Ti NC_003065 Agrobacterium tumefaciens str. C58 214233 57 44 94 139735 139481 − MOBQ
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aThis list is the result of a TBLASTN analysis using the amino acid sequence of HUα or HUβ as a query under strict conditions (i.e., thresholds of 30% identity and 70% query coverage).

bAverage G+C content of the plasmid.

cReported TBLASTN identity to HU.

dPlasmid classification according to its source organism (−, Gram-negative plasmid; +, Gram-positive plasmid).

ePlasmid classification according to its relaxase gene sequence as described by Garcillán-Barcia et al. [16].

Table 3.

Plasmids containing the gene encoding IHF homologa.

Plasmid name Accession no. Source organism Length (nt) G+C content (%)b Identity (%)c Query coverage (%) Subject start Subject end Classificationd MOB familye
At NC_003064 Agrobacterium tumefaciens str. C58 542868 57 36 82 112654 112412 − MOBQ
Megaplasmid NC_012811 Methylobacterium extorquens AM1 1261460 68 33 94 720582 720860 −
p2META1 NC_012809 Methylobacterium extorquens AM1 37858 65 44 95 28369 28635 − MOBQ
pAACI01 NC_013206 Alicyclobacillus acidocaldarius subsp. acidocaldarius DSM 446 91726 54 43 80 62668 62432 +
pACHL01 NC_011879 Arthrobacter chlorophenolicus A6 426858 64 32 92 408818 408546 +
pALVIN02 NC_013862 Allochromatium vinosum DSM 180 39929 53 60 98 10902 10627 −
pAph01 NC_013193 Candidatus Accumulibacter phosphatis clade IIA str. UW-1 167595 62 56 95 144197 144463 − MOBP
pAph03 NC_013191 Candidatus Accumulibacter phosphatis clade IIA str. UW-1 37695 59 58 97 5412 5140 −
pAtK84b NC_011990 Agrobacterium radiobacter K84 184668 59 38 86 54109 53855 − MOBQ
pAtK84c NC_011987 Agrobacterium radiobacter K84 388169 57 43 93 340807 340532 −
46 93 10327 10052
pAtS4b NC_011991 Agrobacterium vitis S4 130435 56 47 97 44880 45152 − MOBQ
pBBta01 NC_009475 Bradyrhizobium sp. BTAi1 228826 61 39 86 6642 6388 −
pBFY46 NC_006297 Bacteroides fragilis YCH46 33716 34 35 89 25098 25343 − MOBP
pBIND01 NC_010580 Beijerinckia indica subsp. indica ATCC 9039 181736 56 36 77 179816 179601 − MOBF
pCHQ1 NC_014007 Sphingobium japonicum UT26S 190974 63 36 90 63111 63377 −
pGLOV01 NC_010815 Geobacter lovleyi SZ 77113 53 38 92 41196 41468 −
pM44601 NC_010373 Methylobacterium sp. 4-46 57951 65 35 97 7806 7534 −
pMPOP01 NC_010727 Methylobacterium populi BJ001 25164 65 49 93 10635 10375 −
pMRAD03 NC_010514 Methylobacterium radiotolerans JCM 2831 42985 63 38 94 26778 26515 − MOBF
pMRAD04 NC_010517 Methylobacterium radiotolerans JCM 2831 37743 64 38 94 10763 10500 −
pPRO1 NC_008607 Pelobacter propionicus DSM 2379 202397 48 41 94 129679 129957 −
pRSPA01 NC_009429 Rhodobacter sphaeroides ATCC 17025 877879 68 49 97 783519 783791 −
pSWIT01 NC_009507 Sphingomonas wittichii RW1 310228 64 40 95 106554 106820 − MOBF
36 92 35341 35069
pTcM1 NC_010600 Acidithiobacillus caldus 65158 57 56 89 25186 25449 − MOBP, MOBQ
pXCV183 NC_007507 Xanthomonas campestris pv. vesicatoria str. 85-10 182572 60 33 95 138753 138490 −
Ti NC_002377 Agrobacterium tumefaciens 194140 55 43 97 180164 180436 − MOBQ
Ti plasmid pTiBo542 NC_010929 Agrobacterium tumefaciens 244978 55 36 86 209743 209489 − MOBQ
45 98 187204 187479
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aThis list is the result of a TBLASTN analysis using the amino acid sequence of IHFα or IHFβ as a query under strict conditions (i.e., thresholds of 30% identity and 70% query coverage).

bAverage G+C content of the plasmid.

cReported TBLASTN identity to IHF.

dPlasmid classification according to its source organism (−, Gram-negative plasmid; +, Gram-positive plasmid).

ePlasmid classification according to its relaxase gene sequence as described by Garcillán-Barcia et al. [16].

Table 4.

Plasmids containing the gene encoding Lrp homologa.

Plasmid name Accession no. Source organism Length (nt) G+C content (%)b Identity (%)c Query coverage (%) Subject start Subject end Classificationd MOB familye
1 NC_008688 Paracoccus denitrificans PD1222 653815 67 41 92 252075 251623 −
42 93 464218 464673
36 96 639341 639811
37 85 110140 109724
A NC_009007 Rhodobacter sphaeroides 2.4.1 114045 69 39 93 30241 29789 − MOBF
B NC_007488 Rhodobacter sphaeroides 2.4.1 114178 70 43 96 81861 81385 −
bglu_1p NC_012723 Burkholderia glumae BGR1 133591 61 36 90 124017 123577 −
Megaplasmid NC_008043 Ruegeria sp. TM1040 821788 59 41 84 143820 144233 −
41 91 687257 687706
36 91 734136 733690
Megaplasmid NC_007974 Cupriavidus metallidurans CH34 2580084 64 44 88 1171245 1170814 − MOBV
40 91 1169702 1169256
38 97 1586726 1586250
Megaplasmid NC_006569 Ruegeria pomeroyi DSS-3 491611 63 36 88 356303 355869 − MOBC
Megaplasmid NC_007336 Ralstonia eutropha JMP134 634917 61 35 93 377503 377045 −
p42e NC_007765 Rhizobium etli CFN 42 505334 62 34 71 255037 255384 −
p42f NC_007766 Rhizobium etli CFN 42 642517 61 45 88 436907 437341 −
43 91 406350 405901
41 85 491383 491799
39 95 210634 211098
39 96 199426 199899
pAB510a NC_013855 Azospirillum sp. B510 1455109 68 57 88 274908 275342 −
44 95 979549 980013
32 94 1180335 1179874
pAB510b NC_013856 Azospirillum sp. B510 723779 67 44 84 471830 472243 −
32 94 318139 318600
pAB510c NC_013857 Azospirillum sp. B510 681723 67 45 85 408064 407645 −
34 91 36385 36834
pAB510d NC_013858 Azospirillum sp. B510 628837 68 44 79 472768 472379 −
40 90 323184 322741
37 87 281438 281866
30 85 619027 618623
pAtS4e NC_011981 Agrobacterium vitis S4 631775 57 30 87 460443 460871 − MOBQ
34 74 425247 424888
pBPHY01 NC_010625 Burkholderia phymatum STM815 1904893 62 46 85 1153608 1154027 −
pBPHY02 NC_010627 Burkholderia phymatum STM815 595108 59 41 91 271795 271346 −
pC NC_010997 Rhizobium etli CIAT 652 1091523 61 46 88 617696 618130 − MOBQ
42 90 609059 608619
39 95 417738 418202
42 79 714804 715193
39 93 406570 407025
pCAUL01 NC_010335 Caulobacter sp. K31 233649 67 34 89 182479 182042 − MOBQ
pEST4011 NC_005793 Achromobacter denitrificans 76958 62 58 88 41224 40793 − MOBP
58 88 34233 33802
pGMI1000MP NC_003296 Ralstonia solanacearum GMI1000 2094509 67 43 98 1737958 1738437 −
46 93 822030 821572
pHV4 NC_013966 Haloferax volcanii DS2 635786 62 33 71 401763 401410 Archaea
pIJB1 NC_013666 Burkholderia cepacia 99448 63 58 88 74907 75338 − MOBP
pK2044 NC_006625 Klebsiella pneumoniae NTUH-K2044 224152 50 33 90 194643 195086 −
pLVPK NC_005249 Klebsiella pneumoniae 219385 50 33 90 46236 46679 −
pMLa NC_002679 Mesorhizobium loti MAFF303099 351911 59 32 93 185603 185148 −
30 89 207314 206877
pMLb NC_002682 Mesorhizobium loti MAFF303099 208315 60 37 93 24632 24177 −
pNGR234a NC_000914 Rhizobium sp. NGR234 536165 58 41 70 197189 196845 − MOBQ
30 89 188867 188430
pNGR234b NC_012586 Rhizobium sp. NGR234 2430033 62 46 90 656547 656107 − MOBQ
45 85 667494 667913
43 90 1038020 1038463
44 85 682796 683215
38 96 2400849 2401319
44 79 709104 708715
41 89 28336 28761
33 89 1108900 1109337
36 90 703213 702764
32 77 1112953 1112582
pPNAP04 NC_008760 Polaromonas naphthalenivorans CJ2 143747 59 35 90 142511 142068 −
pR132501 NC_012848 Rhizobium leguminosarum bv. trifolii WSM1325 828924 60 47 88 234905 234471 − MOBQ
44 86 386338 386760
39 93 645542 645087
42 79 147165 146776
pRALTA NC_010529 Cupriavidus taiwanensis 557200 60 38 91 465839 465393 −
pRHL1 NC_008269 Rhodococcus jostii RHA1 1123075 65 36 91 854207 854656 +
33 84 783666 783253
pRL12 NC_008378 Rhizobium leguminosarum bv. viciae 3841 870021 61 46 88 599116 598682 − MOBQ
43 88 658287 658718
39 93 45601 45146
42 79 450080 449691
pRL8 NC_008383 Rhizobium leguminosarum bv. viciae 3841 147463 59 33 87 70763 70344 − MOBQ
pRLG201 NC_011368 Rhizobium leguminosarum bv. trifolii WSM2304 1266105 60 45 89 917573 917136 − MOBQ
44 85 41998 42417
44 79 473039 472650
40 93 1162146 1161691
40 93 1150939 1150484
32 88 707587 707162
pRSKD131A NC_011962 Rhodobacter sphaeroides KD131 157345 70 42 96 148295 147819 −
pRSKD131B NC_011960 Rhodobacter sphaeroides KD131 103355 70 39 93 98400 97948 −
pRSPA01 NC_009429 Rhodobacter sphaeroides ATCC 17025 877879 68 40 90 31309 30866 −
39 88 659383 658952
pRSPH01 NC_009040 Rhodobacter sphaeroides ATCC 17029 122606 70 39 93 118088 118540 −
pSMED01 NC_009620 Sinorhizobium medicae WSM419 1570951 61 40 77 143180 143557 − MOBQ
34 89 574284 573847
pSMED02 NC_009621 Sinorhizobium medicae WSM419 1245408 60 42 91 556486 556932 − MOBQ
40 91 842324 842758
31 87 22345 21917
pSMED03 NC_009622 Sinorhizobium medicae WSM419 219313 60 46 95 105044 105508 −
pSmeSM11a NC_013545 Sinorhizobium meliloti 144170 60 46 96 70449 70922 − MOBQ
pSymA NC_003037 Sinorhizobium meliloti 1021 1354226 60 43 89 1060699 1060262 − MOBQ
pSymB NC_003078 Sinorhizobium meliloti 1021 1683333 62 38 90 440778 440335 − MOBQ
36 89 29555 29992
pTiS4 NC_011982 Agrobacterium vitis S4 258824 57 42 79 96920 97309 − MOBQ
Unnamed NC_011961 Thermomicrobium roseum DSM 5159 917738 66 30 85 736739 737146 − MOBP
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aThis list is the result of a TBLASTN analysis using the amino acid sequence of Lrp as a query under strict conditions (i.e., thresholds of 30% identity and 70% query coverage).

bAverage G+C content of the plasmid.

cReported TBLASTN identity to Lrp.

dPlasmid classification according to its source organism (−, Gram-negative plasmid; +, Gram-positive plasmid).

ePlasmid classification according to its relaxase gene sequence as described by Garcillán-Barcia et al. [16].

Table 5.

Plasmids containing the gene encoding MvaT or NdpA homologa.

Plasmid name Accession no. Source organism Length (nt) G+C content (%)b Identity (%)c Query coverage (%) Subject start Subject end Classificationd MOB familye
MvaT
pCAR1 NC_004444 Pseudomonas resinovorans 199035 56 61 98 77640 77993 − MOBH
pQBR103 NC_009444 Pseudomonas fluorescens SBW25 425094 53 61 96 98076 97717 −
pWW53 NC_008275 Pseudomonas putida 107929 57 61 98 8415 8768 −
NdpA
p0908 NC_010113 Vibrio sp. 0908 81413 49 51 99 79731 78736 −
pCAR1 NC_004444 Pseudomonas resinovorans 199035 56 36 98 95390 94395 − MOBH
pQBR103 NC_009444 Pseudomonas fluorescens SBW25 425094 53 31 99 161413 160400 −
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aThis list is the result of a TBLASTN analysis using the amino acid sequence of MvaT or NdpA as a query under strict conditions (i.e., thresholds of 30% identity and 70% query coverage).

bAverage G+C content of the plasmid.

cReported TBLASTN identity to MvaT or NdpA.

dPlasmid classification according to its source organism (−, Gram-negative plasmid).

ePlasmid classification according to its relaxase gene sequence as described by Garcillán-Barcia et al. [16].

3.3. Relationships between Plasmid Size and NAP Gene Homolog Distributions

We first compared the sizes of 136 plasmids with NAP gene homologs with those of all 1382 Gram-negative group plasmids. All 1382 plasmids could be divided into 4 groups according to size, small (<10 kb), intermediate (10 to 100 kb), large (100 kb to 1 Mb), and mega (>1 Mb) plasmids. The distribution of the 136 plasmids, each of which had one or more genes encoding NAP homologs, is shown in Figure 1(a): none of 415 small plasmids, 34 (5%) of 686 intermediate plasmids, 90 (33%) of 269 large plasmids, and 12 (100%) of 12 mega plasmids carried at least one NAP gene homolog. The average size of the 136 plasmids was larger (364 kb) than that of all 1382 plasmids (83 kb). These results suggest that larger plasmids, especially >100 kb, frequently have NAP gene homologs. Carrying large plasmids may reduce host fitness more than carrying small plasmids because the former have more genes that can disrupt transcriptional networks in the host cell. In addition, large plasmids may have more binding sites for NAPs than small plasmids. Because chromosome-encoded NAPs bind to both chromosomes and plasmids, carrying large plasmids may also result in a reduction in the binding of NAPs to the host chromosome, causing undesirable effects on the host cell. Plasmid-encoded NAP homologs may interact with chromosome-encoded NAPs, coordinately sustain the structure of both chromosome and plasmid, and regulate the transcriptional regulation network [23]. In fact, recent studies have shown that some plasmid-encoded NAP homologs can complement the depletion of chromosomal NAPs and optimize gene transcription both on plasmids and in the host chromosome [14, 15, 24]. Thus, larger plasmids may have NAP gene homologs to maintain host cell fitness. In addition, the average size of the 38 plasmids containing more than one NAP gene homolog was larger (790 kb) than that of the 98 plasmids containing only one NAP gene homolog (199 kb). This suggests that particularly large plasmids have many NAP gene homologs to maintain themselves in the host cell.

Figure 1.

Figure 1

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Size comparison of the Gram-negative plasmids with and without NAP gene homologs. (a) A total of 136 Gram-negative plasmids with one or more NAP gene homologs and 1246 Gram-negative plasmids without NAP gene homologs are shown by black and white bars, respectively. (b) Gram-negative plasmids with each NAP gene homolog are as follows: H-NS, red; HU, blue; IHF, green; Lrp, purple; MvaT, yellow; and NdpA, orange.

Distributions of the NAP genes on proteobacterial genomes were also surveyed using the TBLASTN program. The average size of the completely sequenced bacterial genomes was 3.25 Mb and 1054 NAP genes (100, Fis; 125, H-NS; 236, HU; 247, IHF; 127, Lrp; 119, MvaT; and 100, NdpA) were found in 588 proteobacterial genomes. Frequency of NAP genes in plasmids was higher (1 per 236 kb) than that in proteobacterial genomes (1 per 1.8 Mb), also suggesting that larger plasmids frequently have NAP gene homologs to minimize their negative effects on the host cell.

Of the plasmids with the NAP gene homolog, the average size of those with the H-NS gene homolog was relatively small (132 kb) while that of those with the Lrp gene homolog was relatively large (725 kb). The average sizes of those with the other NAP gene homologs were as follows: HU (301 kb), IHF (230 kb), MvaT (244 kb), and NdpA (235 kb) (Figure 1(b)). H-NS exists in an oligomeric form and binds to DNA, especially A+T-rich regions, by bridging it [25]. This function may be important for regulating gene expression on relatively small plasmids among those with the NAP gene homolog. The activity of H-NS can also be modulated by Hha-like proteins [26]. Intriguingly, TBLASTN analysis showed that 12 (55%) of 22 plasmids with the H-NS gene homolog also carried gene encoding Hha-like protein although only 65 (5%) of all 1382 plasmids carried Hha-like protein gene (Table 6). This suggests the close relationship of H-NS and Hha-like protein. On the other hand, Lrp exists in dimeric, octameric, and hexadecameric forms and compacts DNA by wrapping it [27]. This distinctive DNA-binding ability may be essential for maintaining the structure of particularly larger plasmids.

Table 6.

Gram-negative plasmids containing the gene encoding Hha-like proteina.

Plasmid name Accession no. Source organism Length (nt) G+C content (%)b NAP gene homolog Identity (%)c Query coverage (%) Subject start Subject end MOB familyd
55989p NC_011752 Escherichia coli 55989 72482 46 53 92 10025 9828
NR1 NC_009133 Escherichia coli 94289 52 53 92 87193 87390 MOBF
p1658/97 NC_004998 Escherichia coli 125491 51 55 92 36419 36616 MOBF
p1ESCUM NC_011749 Escherichia coli UMN026 122301 50 53 92 53508 53311 MOBF
p2ESCUM NC_011739 Escherichia coli UMN026 33809 42 62 90 7682 7488 MOBQ
p53638_226 NC_010719 Escherichia coli 53638 225683 48 55 92 67615 67418 MOBF
pAPEC-O1-R NC_009838 Escherichia coli APEC O1 241387 46 50 92 61389 61586 MOBH
pAPEC-O2-ColV NC_007675 Escherichia coli 184501 49 55 92 3882 3685 MOBF
pAPEC-O2-R NC_006671 Escherichia coli 101375 53 53 92 4856 4659 MOBF
pBS512_211 NC_010660 Shigella boydii CDC 3083-94 210919 46 55 89 190719 190910 MOBF
pBS512_33 NC_010657 Shigella boydii CDC 3083-94 33103 41 62 90 2894 3088
pC15-1a NC_005327 Escherichia coli 92353 53 53 92 87490 87687 MOBF
pCP301 NC_004851 Shigella flexneri 2a str. 301 221618 46 55 92 207828 208025 MOBF
pCROD1 NC_013717 Citrobacter rodentium ICC168 54449 47 56 92 53220 53417
pCROD2 NC_013718 Citrobacter rodentium ICC168 39265 42 62 90 15526 15332
pCT02021853_74 NC_011204 Salmonella enterica subsp. enterica serovar Dublin str. CT_02021853 74551 49 62 90 48482 48288 MOBQ
pCTX-M3 NC_004464 Citrobacter freundii 89468 51 38 71 26136 26294 MOBP
89468 31 96 40648 40439
pCTXM360 NC_011641 Klebsiella pneumoniae 68018 51 38 71 64551 64709 MOBP
68018 31 96 10927 10718
pCVM29188_146 NC_011076 Salmonella enterica subsp. enterica serovar Kentucky str. CVM29188 146811 49 53 92 18755 18558 MOBF
pEC14_114 NC_013175 Escherichia coli 114222 51 53 92 113985 114182 MOBF
pEC-IMP NC_012555 Enterobacter cloacae 318782 48 H-NS 50 92 60491 60688 MOBH
pEC-IMPQ NC_012556 Enterobacter cloacae 324503 48 H-NS 50 92 60491 60688 MOBH
pEG356 NC_013727 Shigella sonnei 70275 52 53 92 69444 69641 MOBF
pEK499 NC_013122 Escherichia coli 117536 53 53 92 41985 42182
pEK516 NC_013121 Escherichia coli 64471 53 53 92 31410 31213
pEL60 NC_005246 Erwinia amylovora 60145 51 38 71 23187 23345 MOBP
60145 31 96 37863 37654
pEntH10407 NC_013507 Escherichia coli ETEC H10407 67094 51 55 78 43421 43254 MOBF
pHCM1 NC_003384 Salmonella enterica subsp. enterica serovar Typhi str. CT18 218160 48 H-NS 47 100 105911 106117 MOBH
pK2044 NC_006625 Klebsiella pneumoniae NTUH-K2044 224152 50 H-NS, Lrp 45 85 143331 143528
pK29 NC_010870 Klebsiella pneumoniae 269674 46 50 92 59322 59519 MOBH
pKF3-70 NC_013542 Klebsiella pneumoniae 70057 52 53 92 15967 15770 MOBF
pKF3-94 NC_013950 Klebsiella pneumoniae 94219 52 58 96 9596 9390 MOBF
pKP187 NC_011282 Klebsiella pneumoniae 342 187922 47 64 96 110083 109877
187922 42 89 1550 1344
pKPN3 NC_009649 Klebsiella pneumoniae subsp. pneumoniae MGH 78578 175879 52 59 97 56930 56721 MOBF
plasmid_153 kb NC_009705 Yersinia pseudotuberculosis IP 31758 153140 40 H-NS 69 93 63342 63542
153140 56 92 49734 49931
pLVPK NC_005249 Klebsiella pneumoniae 219385 50 H-NS, Lrp 61 97 148056 147847
219385 45 85 214828 215025
pMAK1 NC_009981 Salmonella enterica subsp. enterica serovar Choleraesuis 208409 47 H-NS 47 100 49208 49414 MOBH
pMAS2027 NC_013503 Escherichia coli 42644 43 62 90 19685 19491 MOBQ
pO103 NC_013354 Escherichia coli O103:H2 str. 12009 75546 49 55 92 51727 51924 MOBF
pO111_1 NC_013365 Escherichia coli O111:H- str. 11128 204604 47 H-NS 47 100 66925 67131 MOBH
pO111_3 NC_013366 Escherichia coli O111:H- str. 11128 77690 50 55 92 11975 12172 MOBF
pO157 NC_013010 Escherichia coli O157:H7 str. TW14359 94601 48 55 92 70792 70989
pO157 NC_011350 Escherichia coli O157:H7 str. EC4115 94644 48 55 92 54735 54932
pO157 NC_007414 Escherichia coli O157:H7 EDL933 92077 48 55 92 1667 1864
pO157 NC_002128 Escherichia coli O157:H7 str. Sakai 92721 48 55 92 71183 71380
pO26I NC_011812 Escherichia coli 72946 51 53 92 66608 66805 MOBF
pO86A1 NC_008460 Escherichia coli 120730 49 55 92 101598 101795 MOBF
pOLA52 NC_010378 Escherichia coli 51602 46 62 90 12114 11920 MOBQ
pOU1114 NC_010421 Salmonella enterica subsp. enterica serovar Dublin 34595 41 62 90 5446 5252 MOBQ
pOU1115 NC_010422 Salmonella enterica subsp. enterica serovar Dublin 74589 49 62 90 37246 37052 MOBQ
pSB4_227 NC_007608 Shigella boydii Sb227 126697 47 55 92 110688 110885 MOBF
pSE11-1 NC_011419 Escherichia coli SE11 100021 50 56 92 58407 58210 MOBP
pSE34 NC_010860 Salmonella enterica subsp. enterica serovar Enteritidis 32950 41 62 90 21875 22069 MOBQ
pSFO157 NC_009602 Escherichia coli 121239 50 52 75 1709 1870 MOBF
pSG1 NC_007713 Sodalis glossinidius str. “morsitans” 83306 49 H-NS 48 92 2294 2491
pSG1 NC_007182 Sodalis glossinidius 81553 49 48 92 56217 56414
pSMS35_130 NC_010488 Escherichia coli SMS-3-5 130440 51 55 92 3364 3167 MOBF
pSS_046 NC_007385 Shigella sonnei Ss046 214396 45 55 92 178363 178560 MOBF
pUTI89 NC_007941 Escherichia coli UTI89 114230 51 53 92 113993 114190 MOBF
pWR501 NC_002698 Shigella flexneri 221851 46 55 92 207534 207731 MOBF
R100 NC_002134 Shigella flexneri 2b str. 222 94281 52 53 92 87185 87382 MOBF
R27 NC_002305 Salmonella enterica subsp. enterica serovar Typhi 180461 46 H-NS 47 100 159402 159196 MOBH
R478 NC_005211 Serratia marcescens 274762 46 H-NS 50 92 59426 59623 MOBH
R721 NC_002525 Escherichia coli 75582 43 66 90 35285 35091
Unnamed NC_011148 Salmonella enterica subsp. enterica serovar Agona str. SL483 37978 41 H-NS 42 93 1363 1163
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aThis list is the result of a TBLASTN analysis using the amino acid sequence of Hha as a query under strict conditions (i.e., thresholds of 30% identity and 70% query coverage).

bAverage G+C content of the plasmid.

cReported TBLASTN identity to Hha.

dPlasmid classification according to its relaxase gene sequence as described by Garcillán-Barcia et al. [16].

3.4. Relationships between Plasmid G+C Content and NAP Gene Homolog Distributions

Next, we surveyed the G+C content of the Gram-negative group plasmids with and without NAP gene homologs. The average G+C content of the 136 plasmids with NAP gene homologs was higher (56.4%) than that of all 1382 plasmids (44.8%) (Figure 2(a)). Note that the average G+C content of large and mega plasmids (55.0% and 62.9%, resp.) was higher than that of small and intermediate plasmids (44.8% and 40.4%). Considering that larger plasmids frequently had NAP gene homologs, this seems reasonable. Nevertheless, plasmids with H-NS gene homologs had a lower G+C content (48.3%) than did those with other NAP gene homologs, including HU (54.2%), IHF (58.7%), Lrp (62.3%), MvaT (55.6%), and NdpA (52.9%) (Figure 2(b)). H-NS family protein binds A+T-rich regions not only on chromosomes but also on plasmids [15]. Acquisition of a large A+T-rich plasmid with many H-NS binding sites may result in a reduction in the binding of H-NS to the host chromosome and host cell fitness [14]. It is therefore possible that large A+T-rich plasmids may have to supply another H-NS encoded on themselves to minimize the effect on the host cell. On the other hand, although MvaT-family proteins are the functional homolog of H-NS [10, 15], plasmids containing the MvaT gene homolog were not particularly low in G+C content. Although only three plasmids contained the MvaT gene homolog and thus we cannot discuss this interesting phenomenon in detail, the difference between H-NS and MvaT may be derived from their different origin or host bacteria.

Figure 2.

Figure 2

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G+C content comparison of the Gram-negative plasmids with and without NAP gene homologs. (a) A total of 136 Gram-negative plasmids with one or more NAP gene homologs and 1246 Gram-negative plasmids without NAP gene homologs are shown by black and white bars, respectively. (b) Gram-negative plasmids with each NAP gene homolog are as follows: H-NS, red; HU, blue; IHF, green; Lrp, purple; MvaT, yellow; and NdpA, orange.

3.5. Relationships between Plasmid Transferability and NAP Gene Homolog Distributions

Conjugative transfer is an essential function of plasmids, through which they play an important role in bacterial evolution and host cell behavior [11, 12]. Relaxase is an essential protein for plasmid transmission involved in the cleavage of the transferring DNA at the origin of transfer (oriT) site, and plasmids with relaxase genes are thought to be transmissible. Garcillán-Barcia et al. [16] proposed that transmissible plasmids can be classified into 6 MOB families (MOBC, MOBF, MOBH, MOBP, MOBQ, and MOBV) according to the amino acid sequences of 6 prototype relaxase proteins. MOBF and MOBH families are predominantly composed of conjugative plasmids, also called self-transmissible plasmids, and the other 4 families are composed of both mobilizable and conjugative plasmids. Recent studies have reported that plasmid-encoded H-NS family proteins have a “stealth” function and aide horizontal transfer of plasmids [14, 15]. Other NAPs also act as global transcriptional regulators and may regulate expression of genes involved in plasmid transmission. To discuss the relationship between NAP gene homolog distribution and plasmid transferability, we determined the distribution of genes encoding relaxase proteins in Gram-negative plasmids according to the classification by Garcillán-Barcia et al. [16]. Four hundred and nine (30%) of 1382 Gram-negative plasmids carried relaxase genes, and 71 (17%) of those 409 plasmids carried NAP gene homologs. Note that 71 (52%) of 136 plasmids with NAP gene homologs carried relaxase genes. This indicates that plasmids with NAP gene homologs frequently carried the relaxase genes than did those without NAP gene homologs. This phenomenon may be related to the average size of the plasmids. That of the 409 plasmids with relaxase genes was relatively larger (145 kb) than that of all 1382 plasmids (83 kb), corresponding to the fact that larger plasmids frequently had NAP gene homologs.

Four hundred and nine plasmids were classified into each MOB family (13, MOBC; 128, MOBF; 29, MOBH; 86, MOBP; 131, MOBQ; and 26, MOBV). Plasmid 1 (NC_008545) was classified into both the MOBC and MOBF families. In addition, the MOBP, MOBQ, and MOBV families were partially overlapped as described by Garcillán-Barcia et al. [16]. Seventy-one plasmids with NAP gene homologs were contained in each MOB family (1, MOBC; 11, MOBF; 20, MOBH; 8, MOBP; 30, MOBQ; and 2, MOBV). Intriguingly, 20 (69%) of 29 MOBH-family plasmids encoded some NAP homologs, and most of them were H-NS or HU (Table 7). The MOBH family was composed of predominantly large conjugative plasmids, such as the IncHI1 group of plasmids, suggesting that HU may also contribute to plasmid transmission as does H-NS. Furthermore, 30 (23%) of 131 MOBQ-family plasmids also contained some NAP gene homologs, and 15 (50%) of those carried Lrp gene homologs (Table 8). The MOBQ family was composed of both mobilizable and conjugative plasmids, such as those of Rhizobium and Agrobacterium, implying that Lrp may also affect plasmid conjugation. In the other MOB families, plasmids containing NAP gene homologs were less than 10% (8%, MOBC; 9%, MOBF; 9%, MOBP; and 8%, MOBV). This phenomenon may also be related to the average size of the plasmids contained in each MOB family. MOBH (220 kb) and MOBQ (198 kb) were larger than MOBC (78 kb), MOBF (117 kb), MOBP (87 kb), and MOBV (149 kb). On the other hand, the average G+C content of all plasmids belonging to each MOB family was as follows: MOBC (52%), MOBF (52%), MOBH (51%), MOBP (53%), MOBQ (54%), and MOBV (46%). No relationship between the distribution of NAP gene homologs of each MOB family and the G+C content of plasmids was found.

Table 7.

MOBH-family plasmids of Gram-negative origina.

Plasmid name Accession no. Source organism Length (nt) G+C content (%)b NAP gene homolog Identity (%)c Query coverage (%) Subject start Subject end
1 NC_007949 Polaromonas sp. JS666 360405 57 HU 52 99 61052 60786
1 NC_008573 Shewanella sp. ANA-3 278942 46
2 NC_007950 Polaromonas sp. JS666 338007 60
ICEhin1056 NC_011409 Haemophilus influenzae 59393 39
pAM04528 NC_012693 Salmonella enterica 158213 52 HU 57 99 14067 14333
pAPEC-O1-R NC_009838 Escherichia coli APEC O1 241387 46
pAR060302 NC_012692 Escherichia coli 166530 53 HU 57 99 15755 16021
pAsa4 NC_009349 Aeromonas salmonicida subsp. salmonicida A449 166749 53 HU 60 99 26844 26578
pCAR1 NC_004444 Pseudomonas resinovorans 199035 56 MvaT 61 98 77640 77993
NdpA 36 98 95390 94395
HU 42 99 97809 98075
pEC-IMP NC_012555 Enterobacter cloacae 318782 48 H-NS 64 99 109370 108969
pEC-IMPQ NC_012556 Enterobacter cloacae 324503 48 H-NS 64 99 109370 108969
peH4H NC_012690 Escherichia coli 148105 53 HU 57 99 14067 14333
pHCM1 NC_003384 Salmonella enterica subsp. enterica serovar Typhi str. CT18 218160 48 H-NS 61 99 131861 131460
pIP1202 NC_009141 Yersinia pestis bv. Orientalis str. IP275 182913 53 HU 57 99 14067 14333
pK29 NC_010870 Klebsiella pneumoniae 269674 46
plasmid1 NC_007901 Rhodoferax ferrireducens T118 257447 54
pMAK1 NC_009981 Salmonella enterica subsp. enterica serovar Choleraesuis 208409 47 H-NS 61 99 60046 59645
pMAQU02 NC_008739 Marinobacter aquaeolei VT8 213290 53
pO111_1 NC_013365 Escherichia coli O111:H- str. 11128 204604 47 H-NS 61 99 80175 79774
pP91278 NC_008613 Photobacterium damselae subsp. Piscicida 131520 52 HU 57 99 125918 126184
pP99-018 NC_008612 Photobacterium damselae subsp. piscicida 150157 51 HU 57 99 133314 133580
pRA1 NC_012885 Aeromonas hydrophila 143963 51 HU 58 99 15573 15839
pRp12D01 NC_012855 Ralstonia pickettii 12D 389779 58 HU 37 99 321346 321080
pSN254 NC_009140 Salmonella enterica subsp. enterica serovar Newport str. SL254 176473 53 HU 57 99 14067 14333
pTK9001 NC_013930 Thioalkalivibrio sp. K90mix 240256 62
pYR1 NC_009139 Yersinia ruckeri 158038 51 HU 57 99 15070 15336
R27 NC_002305 Salmonella enterica subsp. enterica serovar Typhi 180461 46 H-NS 61 99 148225 148626
R478 NC_005211 Serratia marcescens 274762 46 H-NS 64 99 111747 111346
Rts1 NC_003905 Proteus vulgaris 217182 46
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aThis list is the result of a TBLASTN analysis using the 300 N-terminal amino acid sequence of protein TraI_R27 as a query under strict conditions (i.e., thresholds of 30% identity and 70% query coverage).

bAverage G+C content of the plasmid.

cReported TBLASTN identity to each NAP.

Table 8.

MOBQ-family plasmids of Gram-negative origina.

Plasmid name Accession no. Source organism Length (nt) G+C content (%)b NAP gene homolog Identity (%)c Query coverage (%) Subject start Subject end
1 NC_008242 Chelativorans sp. BNC1 343931 62 HU 41 94 133932 133678
3 NC_007617 Nitrosospira multiformis ATCC 25196 14159 50
3 NC_007961 Nitrobacter hamburgensis X14 121408 62
At NC_003064 Agrobacterium tumefaciens str. C58 542868 57 IHF 36 82 112654 112412
C NC_010542 Cyanothece sp. ATCC 51142 14685 38
ColE9-J NC_011977 Escherichia coli 7577 50
DN1 NC_002636 Dichelobacter nodosus 5112 62
F plasmid NC_008036 Sphingopyxis alaskensis RB2256 28543 60
p11745 NC_013546 Actinobacillus pleuropneumoniae 5486 38
p12494 NC_010889 Actinobacillus pleuropneumoniae 14393 33
p1ABAYE NC_010401 Acinetobacter baumannii AYE 5644 35
p1META1 NC_012807 Methylobacterium extorquens AM1 44195 68
p1METDI NC_012987 Methylobacterium extorquens DM4 141504 65
p2007057 NC_011897 Salmonella enterica subsp. enterica serovar Bovismorbificans 4270 47
p2ABSDF NC_010396 Acinetobacter baumannii SDF 25014 35
p2ESCUM NC_011739 Escherichia coli UMN026 33809 42
p2META1 NC_012809 Methylobacterium extorquens AM1 37858 65 IHF 44 95 28369 28635
p3ABSDF NC_010398 Acinetobacter baumannii SDF 24922 34
p42a NC_007762 Rhizobium etli CFN 42 194229 58
p49879.1 NC_006907 Leptospirillum ferrooxidans 28878 58 HU 47 99 3281 3015
p49879.2 NC_006909 Leptospirillum ferrooxidans 28012 55 HU 48 99 15858 15592
pAb5S9 NC_009476 Aeromonas bestiarum 24716 54
pACRY07 NC_009473 Acidiphilium cryptum JF-5 5629 58
pAgK84 NC_011994 Agrobacterium radiobacter K84 44420 54
pAM5 NC_008691 Acidiphilium multivorum 5161 58
pAMI2 NC_010847 Paracoccus aminophilus 18563 62
pAMI3 NC_013513 Paracoccus aminophilus 5575 61
pAPA01-030 NC_013212 Acetobacter pasteurianus IFO 3283-01 49961 54
pAPA01-040 NC_013213 Acetobacter pasteurianus IFO 3283-01 3204 54
pAtK84b NC_011990 Agrobacterium radiobacter K84 184668 59 IHF 38 86 54109 53855
pAtS4b NC_011991 Agrobacterium vitis S4 130435 56 IHF 47 97 44880 45152
pAtS4c NC_011984 Agrobacterium vitis S4 211620 59 HU 45 94 141245 140991
pAtS4e NC_011981 Agrobacterium vitis S4 631775 57 HU 41 94 40476 40222
Lrp 30 87 460443 460871
Lrp 34 74 425247 424888
pAV2 NC_010310 Acinetobacter venetianus 15135 36
pB NC_010996 Rhizobium etli CIAT 652 429111 58
pBGR3 NC_012847 Bartonella grahamii as4aup 28192 36
pBS512_5 NC_010659 Shigella boydii CDC 3083-94 5114 46
pC NC_010997 Rhizobium etli CIAT 652 1091523 61 Lrp 46 88 617696 618130
Lrp 42 90 609059 608619
Lrp 39 95 417738 418202
Lrp 42 79 714804 715193
Lrp 39 93 406570 407025
pCAUL01 NC_010335 Caulobacter sp. K31 233649 67 HU 44 99 97598 97329
Lrp 34 89 182479 182042
pCAUL02 NC_010333 Caulobacter sp. K31 177878 64
pCCK1900 NC_011378 Pasteurella multocida 10226 61
pCCK381 NC_006994 Pasteurella multocida 10874 61
pCFPG4 NC_011563 Candidatus Azobacteroides pseudotrichonympha genomovar. CFP2 4149 44
pCHE-A NC_012006 Enterobacter cloacae 7560 60
pColE8 NC_012882 Escherichia coli 6751 51
pCROD3 NC_013719 Citrobacter rodentium ICC168 3910 51
pCT02021853_74 NC_011204 Salmonella enterica subsp. enterica serovar Dublin str. CT_02021853 74551 49
pCVM19633_4 NC_011093 Salmonella enterica subsp. enterica serovar Schwarzengrund str. CVM19633 4585 48
pDSHI01 NC_009955 Dinoroseobacter shibae DFL 12 190506 60
pET09 NC_010695 Erwinia tasmaniensis Et1/99 9299 47
pGDIA01 NC_011367 Gluconacetobacter diazotrophicus PAl 5 27455 59
pGOX3 NC_006674 Gluconobacter oxydans 621H 14547 56
pHCG3 NC_005873 Oligotropha carboxidovorans OM5 133058 61
pHRM2a NC_012109 Desulfobacterium autotrophicum HRM2 68709 42
pIGJC156 NC_009781 Escherichia coli 5146 47
pIGMS5 NC_010883 Escherichia coli 6750 51
pIGWZ12 NC_010885 Escherichia coli 4072 50
pISP3 NC_013970 Sphingomonas sp. MM-1 43398 63
pJD4 NC_002098 Neisseria gonorrhoeae 7426 38
plasmid1 NC_007801 Jannaschia sp. CCS1 86072 58
pLD-TEX-KL NC_009966 Fluoribacter dumoffii 66512 39
pMAC NC_006877 Acinetobacter baumannii 9540 35
pMAS2027 NC_013503 Escherichia coli 42644 43
pMbo4.6 NC_013500 Moraxella bovis 4658 39
pMCHL01 NC_011758 Methylobacterium chloromethanicum CM4 380207 66
pMG160 NC_004527 Rhodobacter blasticus 3431 67
pMG828-2 NC_008487 Escherichia coli 4091 50
pMG828-4 NC_008489 Escherichia coli 7462 48
pMMCU1 NC_013056 Acinetobacter calcoaceticus 8771 35
pMMCU2 NC_013506 Acinetobacter baumannii 10270 36
pMRAD01 NC_010510 Methylobacterium radiotolerans JCM 2831 586164 70
pMS260 NC_005312 Actinobacillus pleuropneumoniae 8124 61
pNGR234a NC_000914 Rhizobium sp. NGR234 536165 59 Lrp 41 70 197189 196845
Lrp 30 89 188867 188430
pNGR234b NC_012586 Rhizobium sp. NGR234 2430033 62 Lrp 46 90 656547 656107
Lrp 45 85 667494 667913
Lrp 43 90 1038020 1038463
Lrp 44 85 682796 683215
Lrp 38 96 2400849 2401319
Lrp 44 79 709104 708715
Lrp 41 89 28336 28761
Lrp 33 89 1108900 1109337
Lrp 36 90 703213 702764
Lrp 32 77 1112953 1112582
pNL2 NC_009427 Novosphingobium aromaticivorans DSM 12444 487268 66
pO111_4 NC_013367 Escherichia coli O111:H- str. 11128 8140 50
pO26-S4 NC_011228 Escherichia coli 6758 51
pOLA52 NC_010378 Escherichia coli 51602 46
pOU1114 NC_010421 Salmonella enterica subsp. enterica serovar Dublin 34595 42
pOU1115 NC_010422 Salmonella enterica subsp. enterica serovar Dublin 74589 49
pP NC_003455 Salmonella enterica subsp. enterica serovar Enteritidis 4301 50
pP742405 NC_011733 Cyanothece sp. PCC 7424 18083 38
pP742406 NC_011734 Cyanothece sp. PCC 7424 15219 40
pPMA4326C NC_005921 Pseudomonas syringae pv. maculicola 8244 53
pPNAP07 NC_008763 Polaromonas naphthalenivorans CJ2 9898 57
pPRO2 NC_008608 Pelobacter propionicus DSM 2379 30722 56
pPT1 NC_002143 Comamonas testosteroni 15398 56
pR132501 NC_012848 Rhizobium leguminosarum bv. trifolii WSM1325 828924 60 Lrp 47 88 234905 234471
Lrp 44 86 386338 386760
Lrp 39 93 645542 645087
Lrp 42 79 147165 146776
pR132502 NC_012858 Rhizobium leguminosarum bv. trifolii WSM1325 660973 61
pR132503 NC_012853 Rhizobium leguminosarum bv. trifolii WSM1325 516088 59 HU 47 94 300662 300916
pR132504 NC_012852 Rhizobium leguminosarum bv. trifolii WSM1325 350312 61
pR132505 NC_012854 Rhizobium leguminosarum bv. trifolii WSM1325 294782 60
pRF NC_007110 Rickettsia felis URRWXCal2 62829 34
pRFdelta NC_007111 Rickettsia felis URRWXCal2 39263 33
pRi1724 NC_002575 Agrobacterium rhizogenes 217594 57
pRi2659 NC_010841 Agrobacterium rhizogenes 185462 58
pRL10 NC_008381 Rhizobium leguminosarum bv. viciae 3841 488135 60
pRL11 NC_008384 Rhizobium leguminosarum bv. viciae 3841 684202 61
pRL12 NC_008378 Rhizobium leguminosarum bv. viciae 3841 870021 61 Lrp 46 88 599116 598682
Lrp 43 88 658287 658718
Lrp 39 93 45601 45146
Lrp 42 79 450080 449691
pRL7 NC_008382 Rhizobium leguminosarum bv. viciae 3841 151564 58 HU 48 94 20484 20230
pRL8 NC_008383 Rhizobium leguminosarum bv. viciae 3841 147463 59 Lrp 33 87 70763 70344
pRLG201 NC_011368 Rhizobium leguminosarum bv. trifolii WSM2304 1266105 60 Lrp 45 89 917573 917136
Lrp 44 85 41998 42417
Lrp 44 79 473039 472650
Lrp 40 93 1162146 1161691
Lrp 40 93 1150939 1150484
Lrp 32 88 707587 707162
pRM NC_010927 Rickettsia monacensis 23486 32
pSC101 NC_002056 Salmonella enterica subsp. enterica serovar Typhimurium 9263 51
pSE11-6 NC_011411 Escherichia coli SE11 4082 49
pSE34 NC_010860 Salmonella enterica subsp. enterica serovar Enteritidis 32950 41
pSMED01 NC_009620 Sinorhizobium medicae WSM419 1570951 62 Lrp 40 77 143180 143557
Lrp 34 89 574284 573847
pSMED02 NC_009621 Sinorhizobium medicae WSM419 1245408 60 Lrp 42 91 556486 556932
Lrp 40 91 842324 842758
Lrp 31 87 22345 21917
pSmeSM11a NC_013545 Sinorhizobium meliloti 144170 60 Lrp 46 96 70449 70922
pSmeSM11b NC_010865 Sinorhizobium meliloti SM11 181251 59
pSMS35_4 NC_010486 Escherichia coli SMS-3-5 4074 50
pSx-Qyy NC_006826 Sphingobium xenophagum 5683 56
pSymA NC_003037 Sinorhizobium meliloti 1021 1354226 60 Lrp
pSymB NC_003078 Sinorhizobium meliloti 1021 1683333 62 Lrp 38 90 440778 440335
Lrp 36 89 29555 29992
pTB3 NC_008388 Roseobacter denitrificans OCh 114 16575 55
pTcM1 NC_010600 Acidithiobacillus caldus 65158 57 IHF 56 89 25186 25449
pTiS4 NC_011982 Agrobacterium vitis S4 258824 57 HU 41 94 27356 27102
HU 40 94 83408 83154
Lrp 42 79 96920 97309
pTi-SAKURA NC_002147 Agrobacterium tumefaciens 206479 56 HU 44 94 95763 95509
pUT1 NC_014005 Sphingobium japonicum UT26S 31776 64
pUT2 NC_014009 Sphingobium japonicum UT26S 5398 61
pXAUT01 NC_009717 Xanthobacter autotrophicus Py2 316164 65
pXCV19 NC_007505 Xanthomonas campestris pv. vesicatoria str. 85-10 19146 60
pXF51 NC_002490 Xylella fastidiosa 9a5c 51158 50
pYAN-1 NC_008246 Sphingobium yanoikuyae 5182 62
pYAN-2 NC_008247 Sphingobium yanoikuyae 4924 64
RSF1010 NC_001740 Escherichia coli 8684 61
Symbiotic plasmid p42d NC_004041 Rhizobium etli CFN 42 371254 58
Ti NC_002377 Agrobacterium tumefaciens 194140 55 IHF 43 97 180164 180436
Ti NC_003065 Agrobacterium tumefaciens str. C58 214233 57 HU 44 94 139735 139481
Ti plasmid pTiBo542 NC_010929 Agrobacterium tumefaciens 244978 55 IHF 36 86 209743 209489
IHF 45 98 187204 187479
Unnamed NC_011143 Phenylobacterium zucineum HLK1 382976 69
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aThis list is the result of a TBLASTN analysis using the 300 N-terminal amino acid sequence of protein MobA_RSF1010 as a query under strict conditions (i.e., thresholds of 30% identity and 70% query coverage).

bAverage G+C content of the plasmid.

cReported TBLASTN identity to each NAP.

3.6. Conclusions

We compared the distribution of NAP gene homologs among plasmids and plasmid features. Larger plasmids frequently had NAP gene homologs, possibly to maintain themselves and host cell fitness. Plasmids with NAP gene homologs also frequently carried relaxase genes. Although this may be related to their relatively larger sizes, together with the fact that NAPs affect global gene regulation, it is likely that NAPs contribute to plasmid transmission. Considering the fact that NAPs encoded on plasmids actually help the host cell to integrate newly acquired genes into host regulatory networks [14, 15], large plasmids with NAP gene homologs may be generally more beneficial not only for the host cell, but also for their own existence.

NAP homologs encoded on plasmids can interact with different types of NAPs encoded on the host chromosome and cooperatively regulate host transcriptional networks. Understanding these mechanisms in more detail will shed light on the meanings of the distributions of NAPs on plasmids and chromosomes. Comprehensive analysis of their binding sites in the host and plasmid genomes will help us to understand the relationships between G+C content and the presence of NAPs. Such information will explain how bacteria adapt and evolve by acquiring foreign genes by HGT.

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