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Journal of Bacteriology, February 2001, p. 1405-1412, Vol. 183, No. 4
Institut für Genetik, Technische
Universität Dresden, D-01062 Dresden,
Germany,1 and Institut für
Mikrobiologie, Eidgenössische Technische Hochschule, CH-8092
Zurich, Switzerland2
Received 8 August 2000/Accepted 27 November 2000
The physical and genetic map of the Bradyrhizobium
japonicum chromosome revealed that nitrogen fixation and
nodulation genes are clustered. Because of the complex interactions
between the bacterium and the plant, we expected this chromosomal
sector to contain additional genes that are involved in the maintenance of an efficient symbiosis. Therefore, we determined the nucleotide sequence of a 410-kb region. The overall G+C nucleotide
content was 59.1%. Using a minimum gene length of 150 nucleotides, 388 open reading frames (ORFs) were selected as coding regions. Thirty-five percent of the predicted proteins showed similarity to proteins of
rhizobia. Sixteen percent were similar only to proteins of other
bacteria. No database match was found for 29%. Repetitive DNA
sequence-derived ORFs accounted for the rest. The sequenced region
contained all nitrogen fixation genes and, apart from nodM, all nodulation genes that were known to exist in B. japonicum. We found several genes that seem to encode transport
systems for ferric citrate, molybdate, or carbon sources. Some of them
are preceded by Nodulation (nod) genes
and nitrogen fixation (nif) genes are the key determinants
in the interaction between rhizobia and their host plants (14,
47). However, other loci influence the efficiency of the
interaction or change the host range. Sequencing of the symbiotic
plasmid of Rhizobium sp. strain NGR234 revealed a gene
cluster that encodes a type III secretion system (22). Secreted proteins are encoded within the same cluster
(95). The closely related Sinorhizobium fredii
carries a type III secretion system as well (51, 61).
Mutations within the secretion systems of the two strains influence
symbiosis in a host-dependent manner. Plant and animal pathogens use
related systems to target proteins to host cells (35), but
such proteins have not been identified in rhizobia.
During symbiosis, rhizobia exclusively rely on the carbon supply from
the plant. Although bacteroids can utilize a wide range of carbon
compounds, dicarboxylic acids are most likely the main carbon and
energy source for bacteroids (45, 83). The main argument
is that several strains that have a defect in the dicarboxylic acid
transport system show a Fix In our earlier work, we established a correlated physical and genetic
map of the Bradyrhizobium japonicum genome (28,
53) and discovered that all known nod and
nif genes were clustered within a chromosomal region of
about 400 kb. Furthermore, we found that the G+C content of these genes
was 58 mol% (76), considerably lower than the 61 to 65 mol% reported for the whole genome (43). Therefore, we
concluded that the symbiotic genes have integrated into the chromosome
after horizontal gene transfer from a different strain. In the absence
of genomic rearrangements, this region might contain more genes
involved in symbiosis. This possibility persuaded us to determine its
nucleotide sequence. Here, we present the analysis of a 410-kb region
and discuss the implications for symbiosis on the basis of selected examples.
Bacterial strains.
Escherichia coli strains
ED8767 (66) and JM101 (62) were used for
propagation of the cosmid library and M13 clones, respectively. B. japonicum strain PSP7 (53) is a mutant
derivative of B. japonicum USDA3I1b110 (hereinafter referred
to as USDA110) that contains additional sites for PacI,
SwaI, and PmeI within the tlpA locus. This strain served as the source for DNA from the symbiotic gene region.
Media and bacterial growth conditions.
E. coli
strains were grown in Luria broth, 2× YT, or M9 minimal medium
(85). B. japonicum was grown in
peptone-salts-yeast extract medium (77).
Vectors.
M13mp18 (69) was digested with
SmaI. Subsequently, a polylinker containing recognition
sites for PacI, SwaI, and PmeI was inserted, yielding M13mp18Pme. M13mp18Pme was used for the preparation of single-stranded DNA for sequencing. The vector Lorist6
(25) was used for the construction of a cosmid library.
DNA protocols and construction of an overlapping cosmid
library.
Standard procedures were used for DNA manipulations
(85). DNA of strain PSP7 was restricted with
SwaI. The DNA fragments were separated by pulsed-field gel
electrophoresis as described previously (53). DNA of the
840-kb fragment that contained all of the known nif and
nod genes was isolated by treatment of the gel slice with
DNA sequencing and assembly.
The minimal set of 16 cosmids
was digested with a total of six different blunt-end-generating enzymes
in independent reactions. From each reaction fragments of three or four
different size ranges (with 500 bp being the smallest size) were
isolated through agarose gel electrophoresis. Fragments were cloned
into M13mp18Pme and sequenced (about 2,900 sequence reactions).
Sequencing was done with dye terminator technology on a model 373A
sequencer from Applied Biosystems. For assembly, the Genetics Computer
Group software package was used. Single-stranded and double-stranded gaps were closed by sequencing of PCR-generated fragments (about 600 sequence reactions).
Nucleotide sequence analysis.
If not otherwise stated, the
Genetics Computer Group software package was used. Blast similarity
searches (2) were done at the National Center for
Biotechnology Information (blast{at}ncbi.nlm.nih.gov). Open reading
frames (ORFs) were annotated by the program Glimmer (12,
84). ATG, GTG, and TTG were allowed as start codons. With the
sequences of ORFs that exhibited similarity to known genes, a new data
set that was used to reanalyze the sequence was generated. Repeated
sequences were included into this set only once. Analysis of the
sequenced region resulted in the identification of a maximal number of
937 ORFs, which were assigned identification (id) numbers. All were
screened for similarity to database entries. Software-assisted
examination of many overlapping ORFs led to a considerable reduction in
the number of putative genes. In general, only the ORFs with the
highest coding probabilities were considered. ORFs with low coding
probabilities were selected if they showed similarity to published
sequences. This was the case for id56f2, id102, id725f2,
id774R2, and id813r1. id56f2 (probability value, 64)
exhibits high similarity to ferredoxins. id102
(frxA; probability value, 97) encodes a ferredoxin-like
protein (16). Expression was demonstrated for
id774r2 (hsfA; probability value, 64 [11]) and id813r1 (nrgB;
probability value, 1 [68]). For id725f2
(nolM; probability value, 5 [59]), no data
are available that could prove its functionality. If overlapping ORFs
had the same coding probability but exhibited no similarity to other
sequences, none of the ORFs was chosen. Because the smallest ORF with
similarity to a published sequence encompassed 159 nucleotides, the
lower limit was set to 150 nucleotides.
0021-9193/01/$04.00+0 DOI: 10.1128/JB.183.4.1405-1412.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.
Potential Symbiosis-Specific Genes Uncovered by Sequencing a
410-Kilobase DNA Region of the Bradyrhizobium
japonicum Chromosome
ABSTRACT
Top
Abstract
Introduction
Materials and Methods
Results and Discussion
References
24/12 promoter elements. A number of putative outer membrane proteins and cell wall-modifying enzymes as well as a type III
secretion system might be involved in the interaction with the host.
INTRODUCTION
Top
Abstract
Introduction
Materials and Methods
Results and Discussion
References
phenotype (7, 17, 19,
79, 94) or are at least strongly impaired in nitrogen fixation
(37).
MATERIALS AND METHODS
Top
Abstract
Introduction
Materials and Methods
Results and Discussion
References
-agarase I (Calbiochem, La Jolla, Calif.). The isolated DNA was
digested partially with Sau3AI. DNA fragments in the size
range 35 to 50 kb were isolated after pulsed-field gel electrophoresis
by treatment with -agarase, followed by further purification with
phenol and a final ethanol precipitation. About 0.2 µg of DNA was
ligated with 0.5 µg of vector DNA (Lorist6) that had been digested
with BamHI and dephosphorylated. DNA was packaged (Gigapack
II Gold packaging extract; Stratagene, La Jolla, Calif.) and transduced
into E. coli ED8767. Selection for kanamycin resistance
yielded more than 250 clones. Two hundred fifty clones were picked and
cultivated in 1 ml of 2× YT. Aliquots of 100 µl were transferred
into microtiter plates prefilled with 100 µl of 50% glycerol. The
plates were sealed and stored. The rest of the culture was used for DNA
isolation. DNA was transferred to nylon membranes and hybridized
against 10 probes from the symbiotic gene region. This led to the
selection of 99 clones. Restriction analysis finally resulted in an
ordered cosmid library consisting of a minimal set of 16 partially
overlapping cosmids encompassing the gene loci from nodVW to
ndp.
54 consensus [20]), (where
"n5" represents any five bases), TTGACA-n17-TATAAT (70 consensus [56]), and
ATCCA-n7-GATG-n6-ATCCAAACAATCGATTTTACCAATC (nod
box; modified from reference 87).
Identification of transmembrane domains and N-terminal signal sequences. Transmembrane domains were searched with TMpred (http://www.ch.embnet.org/software/TMPRED_form.html). Proteins supposed to contain at least one transmembrane domain were analyzed a second time with TopPred2 (http://www.sbc.su.se/~erikw/toppred2). Likewise, the presence of N-terminal signal sequences (67) was investigated first by the program SPscan and second by Signal P (http://www.cbs.dtu.dk/services/SignalP/).
Nucleotide sequence accession number. The nucleotide sequence has been deposited in the EMBL database under accession numbers AF322012 and AF322013.
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RESULTS AND DISCUSSION |
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Abstract
Introduction
Materials and Methods
Results and Discussion
References
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Evaluation of the sequence quality. To analyze the quality on the nucleotide level, the new sequence data were compared with data from past projects. Within more than 10 kb, only two differences were found, and both were due to reading errors in the old sequences. In addition, more than 4 kb was sequenced a second time and independently by a company. Both sequences were identical.
In several cases, for example with hupD, hupH, and noeE, the sequence initially appeared to contain mistakes that caused frameshifts. In all cases, we could rely on high-quality sequence results, thus excluding the possibility of sequencing errors. In hupD it was possible to track the frameshift down to a single nucleotide. The corresponding region was reamplified directly from chromosomal DNA. Sequencing of the PCR fragment confirmed the frameshift. The same procedure was done for the verification of the noeE locus. Based on these data, we expect that the error frequency is less than one mistake per 10,000 bp.Coding capacity of the symbiotic region.
Analysis of the
nucleotide sequence led to the selection of 388 ORFs, depicted in Fig.
1. Surprisingly, only
35% of the ORFs were similar to genes previously described for
rhizobia (Table 1). Apart from having
genes for nodulation, nitrogen fixation, and type III secretion, the
symbiotic island of B. japonicum has little in common with
the symbiotic plasmid of NGR234. This is remarkable because both
strains have overlapping host ranges (they nodulate Macroptilium
atropurpureum and Vigna radiata, for example). Obviously, the two strains follow partially different strategies for
the establishment of an efficient symbiosis. This flexibility may be
promoted by numerous insertion sequence (IS)-like elements that
facilitate recombination events.
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Nodulation genes. The nodulation gene cluster containing nodABC has been characterized previously (27, 59). Id808 has good similarity to NoeI of Rhizobium sp. strain NGR234. In NGR234, NoeI is involved in the 2-O-methylation of the Nod factor at the fucosyl residue (40). Because the Nod factor of B. japonicum also contains a methylated fucosyl residue (86), Id808 may be a homologue of NoeI.
Two deduced proteins of neighboring ORFs (Id853 and Id855) exhibit similarity to different parts of NoeE of Rhizobium sp. strain NGR234. NoeE was shown to have sulfotransferase activity (32, 75). However, no sulfatation of the Nod factor has been described for B. japonicum. The lack of a nod box-containing promoter region raises further doubt about the involvement of id853 and id855 in Nod factor biosynthesis. The only nodulation gene that is known to exist in B. japonicum and that is missing within the sequenced region is nodM, which encodes a glucosamine synthase (5). In B. japonicum, nodM was found next to a region determining genotype-specific nodulation of soybean cultivars (58). Preliminary data suggest that this region is located about 100 kb downstream of nodVW (unpublished).Nitrogen fixation and ferredoxin-like genes. As with nodulation genes, most of the nitrogen fixation genes of B. japonicum had been studied before the onset of this project. The newly identified genes nifQ, nifW, nifZ, and fixU are known from other nitrogen-fixing bacteria, including rhizobia (47). NifW potentially in complex with NifZ may be required for oxygen protection of the nitrogenase (48, 54). The presence of NifQ is not surprising because it seems to be involved in the incorporation of molybdenum into the iron-molybdenum cofactor of nitrogenase (39). Nothing is known about the function of FixU, which has some similarity to NifT of Azotobacter vinelandii.
Interesting is the presence of several ferredoxin-like proteins that are encoded close to nif genes and that are present in other nitrogen-fixing bacteria as well. Carter et al. (10) purified a two-[4Fe-4S]-cluster-containing enzyme from a B. japonicum strain and suggested that it serves as an electron donor for nitrogenase. Based on the reported amino acid composition, the corresponding enzyme may be encoded by id56f2 (fdxN) in USDA110. A similar protein is encoded by frxA (id102). Both proteins contain the cysteine motifs (82) that are typical for ferredoxins with two [4Fe-4S] clusters. In S. meliloti, FdxN is essential for nitrogen fixation (50). In B. japonicum, a mutation of frxA does not significantly change symbiotic nitrogen fixation (16). Furthermore, a large deletion that encompasses fdxN (mutant strain E1-7d1) still fixes nitrogen (31). This finding suggests that both ferredoxins are able to substitute for each other. The ferredoxin encoded by id81 is very similar to ferredoxin III from Rhodobacter capsulatus (44) and FdxB of NGR234 (22). In R. capsulatus, ferredoxin III probably does not serve as an electron donor to nitrogenase (44). Most similar to Id113 is a [2Fe-2S] ferredoxin of Clostridium pasteurianum, which was shown by cross-linking experiments to interact with the MoFe protein of nitrogenase (26).Secretion of fixed nitrogen. Fixed nitrogen might be translocated into the plant cytosol as ammonium (46, 93) or alanine (97). Recently, it was shown that bacteroids of Rhizobium leguminosarum secrete both alanine and ammonium (1). The product of id56 has high similarity to alanine dehydrogenases. Preliminary results suggest that the gene is transcribed under microaerobic conditions, supporting the idea that it may be involved in the formation of alanine that is then secreted.
Hydrogen metabolism. Hydrogenase activity is widespread among Bradyrhizobium strains and has been described for USDA110 as well (9). Thus, it was not surprising to find the hup gene cluster within the symbiotic island. The genes encoding the small and large subunits of hydrogenase (id19 and id22) are highly similar to the corresponding genes of other bacteria. However, changes within the nucleotide sequence and the insertion of a repetitive element led to fragmentation and probably also to the deletion of several other genes. For example, hupG, -I and -J, which are present in R. leguminosarum (AC X52974) as well as in B. japonicum (23), are missing. hypB was split by the insertion of an IS-like element. It will be interesting to see if these changes still allow hydrogenase activity.
Type III secretion system. More than 20 ORFs within a large cluster stretching from id185 to id289 are similar to genes of NGR234. In NGR234, several of these genes are known to be involved in the formation of a type III secretion system (22, 95). Also conserved is id284 (y4x1), whose product has similarity to transcriptional activators of the two-component regulatory family. The regulator seems to be under the control of a nod box-containing promoter sequence, raising the possibility that this cluster is active very early in symbiosis.
Several deduced proteins exhibit similarity to proteins of NGR234 but not to components of type III secretion systems from pathogenic bacteria. They may be part of a specialized transport complex. Alternatively, they might be secreted proteins. In NGR234 two secreted proteins, NolX and Y4xL, were identified (95). The corresponding genes are located downstream of rhcC1 together with six other ORFs. Interestingly, in B. japonicum these genes seem to be absent and only a short ORF (id213) has some similarity to the 5' half of y4xL. Candidates for secreted proteins are of course those that are encoded within the cluster. However, proteins encoded outside of this cluster may also be secreted. Id431 is a leucine-rich repeat protein that has good similarity to IpaH of Shigella flexneri and SspH1 of Salmonella enterica serovar Typhimurium; both were shown to be secreted (13, 63). Id165, Id167, and Id169 have some similarity to different parts of Id431. Id797 has weak similarity to proteins of the bean pathogen Pseudomonas syringae pathovar phaseolicola, one being the avirulence protein AvrPph3 (42) and the other being a virulence protein of unknown function that is encoded within the pathogenicity island (41).Carbon metabolism.
id13 (dctA) encodes a
protein that is highly similar to known C4-dicarboxylate
permeases. The presence of a nod box as well as a 24/12
promoter sequence suggests a complex regulation. Mutations in the two
rpoN genes that encode 54 do not affect the
ability to grow on succinate or malate as a carbon source
(52). There are several possibilities to explain this
result. First, the identified dctA gene may be transcribed in a 54-independent manner. Second, there might be more
than one uptake system. The finding that the deletion mutant E1-7d1, in
which dctA is also removed, is still able to fix nitrogen
(31) supports the latter possibility. Two succinate uptake
systems were reported to exist in B. japonicum 61-A-101
(36).
carbonic anhydrase
that is probably encoded by id818. carbonic anhydrases
are ancient enzymes frequently found in prokaryotes and are required
for efficient CO2 fixation (33, 88).
Alternatively, other enzymes such as phosphoenolpyruvate carboxylase
may utilize the generated HCO3.
Genes that might be involved in metal ion uptake.
The product
of id331 has similarity to citrate-proton symport proteins.
Citrate is a prominent metabolite in soybean nodules and can be used as
a carbon source by bacteroids (90). However, we favor the
idea that the encoded protein is used for the import of
Fe(III)-citrate. Fe(III)-citrate is probably the Fe transport form in
soybean plants (92) and can be imported by bacteroids (65) and used by free-living cells of USDA110
(73). The presence of a 24/12 promoter element
indicates that the ORF may be regulated by 54, which
would guarantee its timely expression together with the nif
genes. Compared to the well-known fec-encoded ABC-type
ferric citrate uptake system (8), the suggested metal
citrate-proton symport would have the advantage that it does not
consume ATP.
24/12 promoter sequences further supports their
possible involvement in symbiosis.
Enzymatic functions that might interact with plant cell wall components. Id568 shows weak similarity to glucuronidases. Similarity is higher between Id636 and polygalacturonases. All four conserved regions that have been proposed to contribute to the catalytic site of polygalacturonase from Erwinia carotovora (72) are present in Id636 as well, suggesting that this protein may have a similar function. A third protein (Id637) is similar to pectin methyl esterases of Arabidopsis thaliana. It is still disputed if such enzymatic functions contribute to the infection process. Early work suggested that pectic enzymes produced by the host play an important part in the infection process (18, 57), but these results have been questioned (38, 55). Later it was shown that rhizobia are indeed able to produce low levels of pectolytic enzymes (34); however, no genes have been identified so far. The fact that all three putative enzymes identified here are predicted to contain N-terminally located signal sequences underlines their potential extracellular function.
Outer membrane proteins.
Outer membrane proteins are the ideal
candidates for mediating the interaction between bacteria and the host.
Id117 has similarity to a family of outer membrane proteins that is
characterized by eight amphipathic strands (6). Id548
has weak similarity to OstA, a protein that contributes to the degree
of organic solvent tolerance in E. coli (3).
Four other proteins (Id352, Id525, Id693, and Id877) are similar to
each other and to Omp31, a major outer membrane protein of
Brucella melitensis that may serve as a porin
(96).
Rhizobitoxine-related function. Id863, Id864, and Id865 have high similarity to RtxA, which is involved in rhizobitoxine production in Bradyrhizobium elkanii (80, 81). Rhizobitoxine influences symbiosis with Glycine max, Vigna radiata, and Macroptilium atropurpureum, probably through inhibition of ethylene production (15, 71, 89, 99). Originally it was discovered due to its potential to induce chlorosis in soybeans (70). The identification of the corresponding genes in USDA110 was surprising because it was reported that this strain does not produce rhizobitoxine (24, 64). This may be due to differences in gene regulation or enzyme function. So far, the biosynthetic pathway for rhizobitoxine synthesis has not been elucidated, and the molecule potentially produced by USDA110 may have a different structure. Downstream of id865 and likely within the same operon, there are five additional ORFs (id863 to id872) that may be involved in the biosynthesis of a rhizobitoxine-like molecule.
The largest protein is probably a peptide synthetase.
The
longest ORF found within the sequenced region may encode a protein of
3,310 amino acids. The protein has high similarity to peptide
synthetases. Like other peptide synthetases, it has a characteristic
order of conserved domains, and 4'-phosphopantetheine probably serves
as carrier of acyl intermediates (reviewed in reference
49). Deduced from the conserved domain structure, Id930
may synthesize a tripeptide; however, the similarity to other
synthetases does not reveal the potential composition of the product.
Interesting is the presence of a 24/12 promoter sequence that was
shown to be functional (98). A gene cluster located a few
kilobases upstream of id930 might be involved in the
synthesis of the phosphopantetheine carrier.
Nineteen percent of the identified ORFs are related to genes
involved in integration and recombination.
According to their
similarities to published sequences, we grouped the integration- and
recombination-related proteins, if appropriate, into the families that
were summarized by Mahillon and Chandler (60). Most
preponderant are members of the IS3, IS5, and
IS21 families. Best conserved are the repeated sequences RS
that belong to the IS630 family. On the amino acid
level, all six copies are identical in length and have at least 99.2% identical amino acid residues. Remarkably, all have the same
orientation. The same orientation is also found for the six elements
that share similarity with reverse transcriptases. However, peptide
lengths and similarities are much more variant. Differences in the G+C contents, 65.8% for id266 and 58% for id776,
suggest that they originate from independent sources.
elements can also occur either spontaneously (31) or after prolonged heat treatment (29).
Does the symbiotic region of B. japonicum result from an integration event? A number of novel genes that fit well into the symbiotic scheme have been identified. Despite the presence of a number of IS-related elements, there is no indication that recombination events led to an insertion of essential housekeeping genes from B. japonicum or to the translocation of essential symbiotic genes to a separate chromosomal location. In cases where genes are present whose functions are known to be required for the free-living bacterium, like groESL, and hemN, they represent nonessential copies of homologues that are present elsewhere in the genome as well (21, 21a). Several genes (id489 to id501) exhibit similarity to a region that was suggested to be involved in the maintenance of plasmid pNL1 of Sphingomonas aromaticivorans (78). Next to this region, a protein (Id523) that is similar to the N terminus of the nicking enzyme TraA is encoded. Genes id489 to id501 are also remarkable because of their high G+C contents of about 65.3%; the sequence stretches that contain the nif (id1 to id149) and nod (id668 to id748) genes have an average G+C content below 58%, suggesting that the symbiotic region is made of pieces from different origins.
So far we have no further evidence that an integration event took place. This is different from the situation in Mesorhizobium loti strain ICMP3153, in which the symbiotic island that can be transferred to other strains integrated into a phenylalanine-specific tRNA gene (91).Perspectives. The established nucleotide sequence significantly facilitates the design of future experiments. In many cases protein functions can be deduced from their similarity to known proteins and tested accordingly. For many ORFs, such similarities do not exist. Therefore, our work will also be directed towards mutational and gene expression analyses of the whole region. This will further increase our knowledge about genes required at different stages during nodule development. For a full understanding of the symbiotic process, however, a detailed knowledge of the complete genome is required.
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ACKNOWLEDGMENTS |
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We thank Monika Weishaupt for technical assistance.
This work was supported by grant 0-20-918-94 from the ETH, Zurich, Switzerland.
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FOOTNOTES |
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* Corresponding author. Mailing address: Institut für Genetik, Technische Universität Dresden, Mommsenstr. 13, D-01062 Dresden, Germany. Phone:(49) 351 4634000. Fax: (49) 351 4637725. E-mail: mgoettfe{at}rcs.urz.tu-dresden.de.
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Abstract
Introduction
Materials and Methods
Results and Discussion
References
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Journal of Bacteriology, February 2001, p. 1405-1412, Vol. 183, No. 4
0021-9193/01/$04.00+0 DOI: 10.1128/JB.183.4.1405-1412.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.
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