Skip to main content
  • Extended genome report
  • Open access
  • Published:

High-quality draft genome sequence of Rhizobium mesoamericanum strain STM6155, a Mimosa pudica microsymbiont from New Caledonia

Abstract

Rhizobium mesoamericanum STM6155 (INSCD = ATYY01000000) is an aerobic, motile, Gram-negative, non-spore-forming rod that can exist as a soil saprophyte or as an effective nitrogen fixing microsymbiont of the legume Mimosa pudica L.. STM6155 was isolated in 2009 from a nodule of the trap host M. pudica grown in nickel-rich soil collected near Mont Dore, New Caledonia. R. mesoamericanum STM6155 was selected as part of the DOE Joint Genome Institute 2010 Genomic Encyclopedia for Bacteria and Archaea-Root Nodule Bacteria (GEBA-RNB) genome sequencing project. Here we describe the symbiotic properties of R. mesoamericanum STM6155, together with its genome sequence information and annotation. The 6,927,906 bp high-quality draft genome is arranged into 147 scaffolds of 152 contigs containing 6855 protein-coding genes and 71 RNA-only encoding genes. Strain STM6155 forms an ANI clique (ID 2435) with the sequenced R. mesoamericanum strain STM3625, and the nodulation genes are highly conserved in these strains and the type strain of Rhizobium grahamii CCGE501T. Within the STM6155 genome, we have identified a chr chromate efflux gene cluster of six genes arranged into two putative operons and we postulate that this cluster is important for the survival of STM6155 in ultramafic soils containing high concentrations of chromate.

Introduction

The ability of legumes to engage in a dinitrogen fixing symbiosis with soil dwelling bacteria, collectively known as rhizobia, has contributed to their success in colonizing nitrogen deficient soils over a broad range of edaphic conditions. While legume crops and pastures make important contributions to agricultural productivity, invasive legume weeds such as Mimosa pudica L. have a negative impact on natural and agricultural ecological systems. M. pudica originates from America [1] and became a highly invasive pantropical weed. It has been identified as a pest species, associated with land degradation, biodiversity loss, and reduced agricultural and therefore economic productivity, with attendant social and health impacts [2]. It requires resource-intensive chemical and mechanical control methods [2]. Conversely, however, it has potential commercial value as a source of silver nanoparticles and pharmacologically active phytochemicals, and as a phytoremediant for arsenic-polluted soils [36]. Understanding the Mimosa symbiosis can therefore help to achieve outcomes such as preventing biodiversity loss and improving the use of terrestrial ecosystems, as well as promoting sustainable industry, which form part of the Sustainable Development Goals adopted in September 2015 as part of the UN’s development agenda ‘Transforming our world: the 2030 Agenda for Sustainable Development’ [7].

M. pudica has the unusual property of interacting with microsymbionts belonging to both alpha- and beta-rhizobia [8, 9]. Alpha-rhizobia are preferred symbionts of most legume species, but beta-rhizobia have a far narrower host range, with a particular affinity for the Mimosa genus in South America [10] and endemic papilionoid species in South Africa [11]. Diversity studies have shown that alpha-rhizobia are found less frequently than beta-rhizobia in the nodules of M. pudica [1217], and nodulating species exhibit different competitive and symbiotic characteristics [18, 19]. M. pudica thus represents an interesting legume species for comparative analyses of symbiotic traits and plant-infection genetic programs in the two categories of symbionts.

M. pudica was introduced to New Caledonia at the end of the 19th century [15]. Rhizobium mesoamericanum STM6155 was isolated from nodules of M. pudica growing in soil characterized by neutral pH (6.8) and very high total nickel concentrations (10.1 g.kg−1) that was collected near the abandoned nickel mining site of Mont Dore (S3: 22°15’16.51”S and 166°36’44.27”E) in New Caledonia [15].

The 16S rRNA and recA house-keeping genes of STM6155 showed 100 and 97% nucleotide identity with their orthologs in Rhizobium mesoamericanum CCGE501T from Mexico [20], and STM6155 was thus tentatively included in the same species. Among described alpha-rhizobial symbionts of M. pudica ( R. etli bv. mimosae, R. tropici and R. mesoamericanum ), R. mesoamericanum is the most frequently detected species, with a distribution on different continents (Central & South America, Asia) [17, 20]. In Mexico, endemic Mimosa spp. growing in weakly acidic, neutral or slightly alkaline soil are preferentially nodulated by Alphaproteobacterial rhizobia, including strains of R. mesoamericanum [21], whereas acid-tolerant Burkholderia spp. are favoured microsymbionts of endemic Mimosa spp., including M. pudica, in acidic Brazilian soils [14, 22]. R. mesoamericanum is much less effective for nitrogen fixation on M. pudica than Burkholderia phymatum STM815 or Cupriavidus taiwanensis STM6070 [12, 15], and much less competitive in comparison to B. phymatum and B. tuberum [19]. These data question how R. mesoamericanum can maintain itself as a symbiont of M. pudica despite its low competitiveness. Strain STM6155 has therefore been selected as part of the DOE Joint Genome Institute 2010 Genomic Encyclopedia for Bacteria and Archaea-Root Nodule Bacteria (GEBA-RNB) sequencing project [23, 24], to investigate the genome traits that enable this species to adapt to a symbiotic and saprophytic lifestyle. Here we present a summary classification and a set of general features for R. mesoamericanum STM6155, together with a description of its genome sequence and annotation.

Organism information

Classification and features

Rhizobium mesoamericanum STM6155 is a motile, Gram-negative, non-spore forming strain in the order Rhizobiales of the class Alphaproteobacteria . The rod-shaped form has dimensions of 0.4–0.6 μm in width and 1.0–1.4 μm in length (Fig. 1 Left and Center). It is fast growing, forming colonies within 3–4 days when grown on half strength Lupin Agar (½LA) [25], tryptone-yeast extract agar (TY) [26] or a modified yeast-mannitol agar [27] at 28 °C. Colonies on ½LA are white-opaque, slightly domed and moderately mucoid with smooth margins (Fig. 1 Right).

Fig. 1
figure 1

Images of Rhizobium mesoamericanum STM6155 using scanning (Left) and transmission (Center) electron microscopy and the appearance of colony morphology on solid media (Right)

Figure 2 shows the phylogenetic relationship of R. mesoamericanum STM6155 in a 16S rRNA sequence based tree. This strain is the most similar to R. mesoamericanum CCGE501T based on the 16S rRNA gene alignment, with sequence identities of 100% over 1362 bp, as determined using the EzTaxon-e database, which contains the sequences of validly published type strains [28]. Minimum Information about the Genome Sequence for STM6155 is provided in Table 1 and Additional file 1: Table S1.

Fig. 2
figure 2

Phylogenetic tree showing the relationship of Rhizobium mesoamericanum STM6155 (shown in bold blue print) to Rhizobium spp. and other root nodule bacteria in the order Rhizobiales based on aligned sequences of the 16S rRNA gene (1286 bp intragenic sequence). Mesorhizobium loti LMG6125T was used as an outgroup. All sites were informative and there were no gap-containing sites. Phylogenetic analyses were performed using MEGA, version 5 [53]. The tree was built using the Maximum-Likelihood method with the General Time Reversible model [54]. Bootstrap analysis [55] with 500 replicates was performed to assess the support of the clusters. Type strains are indicated with a superscript T. Strains with a genome sequencing project registered in GOLD [31] are in bold font and the GOLD ID is provided after the GenBank accession number, where this is available. Finished genomes are indicated with an asterisk

Table 1 Classification and general features of Rhizobium mesoamericanum STM6155 in accordance with the MIGS recommendations [56] published by the Genome Standards Consortium [57]

Symbiotaxonomy

R. mesoamericanum STM6155 was isolated from nodules of M. pudica, as were others members of this species including STM3625, STM3629, tpud40a and tpud22.2 [12, 15, 17]. However, the type strain of the species, CCGE501T, originates from nodules of Phaseolus vulgaris L. [20]. Strain STM6155 forms nodules and fixes N2 with several Mimosa species of American origin, including M. pudica and Mimosa acustipulata Benth. It forms white, ineffective nodules on Mimosa pigra L. and Mimosa caesalpinifolia Benth. but is unable to nodulate Mimosa scabrella Benth. STM6155 is also able to form nitrogen-fixing nodules on P. vulgaris and on a legume, Acacia spirorbis Labill., which grows in the same area from which STM6155 originates [15]. The symbiotic characteristics of R. mesoamericanum STM6155 on a range of hosts are summarised in Additional file 1: Table S2. R. mesoamericanum STM6155 contains a full set of nodulation genes, and exhibits uncommon features, such as the presence of two alleles of the nodA gene in its genome, a feature that seems conserved in several strains of the species such as STM3625 [15, 17, 29].

Genome sequencing information

Genome project history

This organism was selected for sequencing at the U.S. Department of Energy funded Joint Genome Institute as part of the Genomic Encyclopedia of Bacteria and Archaea-Root Nodule Bacteria (GEBA-RNB) project [23, 24]. The root nodule bacteria in this project were selected on the basis of environmental and agricultural relevance to issues in global carbon cycling, alternative energy production, and biogeochemical importance. The genome project is deposited in the Genomes On-Line Database [30] and a high-quality permanent draft genome sequence is deposited in IMG [31]. Sequencing, finishing and annotation were performed by the JGI. A summary of the project information is shown in Table 2.

Table 2 Genome sequencing project information for Rhizobium mesoamericanum STM6155

Growth conditions and genomic DNA preparation

Rhizobium mesoamericanum STM6155 was streaked onto TY solid medium [26] and grown at 28 °C for 3 days to obtain well grown, well separated colonies, then a single colony was selected and used to inoculate 5 ml TY broth medium. The culture was grown for 48 h on a gyratory shaker (200 rpm) at 28 °C. Subsequently 1 ml was used to inoculate 60 ml TY broth medium and the cells were incubated at 28 °C on a gyratory shaker at 200 rpm until an OD600nm of 0.6 was reached. DNA was isolated from 60 ml of cells using a CTAB bacterial genomic DNA isolation method [32]. Final concentration of the DNA was set to 0.5 mg ml-1.

Genome sequencing and assembly

The draft genome of R. mesoamericanum STM6155 was generated at the JGI using Illumina technology [33]. An Illumina standard shotgun library was constructed and sequenced using the Illumina HiSeq 2000 platform which generated 14,034,164 reads totaling 2105 Mbp. All general aspects of library construction and sequencing performed at the JGI can be found on the JGI website [34]. All raw Illumina sequence data was passed through DUK, a filtering program developed at JGI, which removes known Illumina sequencing and library preparation artifacts (Mingkun L, Copeland A, Han J. unpublished), providing 12,829,288 trimmed reads totaling 1924 Mbp. The following steps were then performed for assembly: 1) filtered Illumina reads were assembled using Velvet [35] (version 1.1.04); 2) 1–3 Kbp simulated paired end reads were created from Velvet contigs using wgsim [36]; 3) Illumina reads were assembled with simulated read pairs using Allpaths–LG [37] (version r39750). Parameters for assembly steps were: 1) Velvet (velveth: --v --s 51 --e 71 --i 2 --t 1 --f “-shortPaired -fastq $FASTQ” --o “-ins_length 250 -min_contig_lgth 500”); 2) wgsim -e 0 -1 76 -2 76 -r 0 -R 0 -X 0); 3) Allpaths–LG (PrepareAllpathsInputs:PHRED64 = 1 PLOIDY = 1 FRAGCOVERAGE = 125 JUMPCOVERAGE = 25 LONGJUMPCOV = 50, RunAllpath-sLG: THREADS = 8 RUN = stdshredpairs TARGETS = standard VAPIWARNONLY = True OVERWRITE = True). The final draft assembly contained 152 contigs in 147 scaffolds. The total size of the genome is 6.9 Mbp and the final assembly is based on 1924 Mbp of Illumina data, which provides an average 279x coverage of the genome.

Genome annotation

Genes were identified using Prodigal [38] as part of the DOE-JGI annotation pipeline [39, 40]. The predicted CDSs were translated and used to search the National Center for Biotechnology Information nonredundant database, UniProt, TIGRFam, Pfam, PRIAM, KEGG, COG, and InterPro databases. The tRNAScanSE tool [41] was used to find tRNA genes, whereas ribosomal RNA genes were found by searches against models of the ribosomal RNA genes built from SILVA [42]. Other non–coding RNAs such as the RNA components of the protein secretion complex and the RNase P were identified by searching the genome for the corresponding Rfam profiles using INFERNAL [43]. Additional gene prediction analysis and manual functional annotation was performed within the Integrated Microbial Genomes – Expert Review platform [44] developed by the Joint Genome Institute, Walnut Creek, CA, USA. The annotated genome of R. mesoamericanum STM6155 is available in IMG (genome ID = 2513237088).

Genome properties

The genome is 6,927,906 nucleotides with 58.90% GC content (Table 3) and comprised of 147 scaffolds (selected scaffolds are shown in Fig. 3) of 152 contigs. The location of nodulation (Fig. 3a), nitrogenase (Fig. 3b) and chromate resistance (Fig. 3c) loci on genome scaffolds are shown. From a total of 6926 genes in the genome, 6855 were protein encoding and 71 RNA only encoding genes. The majority of genes (76.02%) were assigned a putative function, whilst the remaining genes were annotated as hypothetical. The distribution of genes into COGs functional categories is presented in Table 4.

Table 3 Genome statistics for Rhizobium mesoamericanum STM6155
Fig. 3
figure 3

Graphical map of selected scaffolds from the genome of Rhizobium mesoamericanum STM6155 containing common nodulation nodABC (a), nitrogenase nifHDK (b) and chromate resistance (chr) (c) clusters. The genes chrY to P correspond to the STM6155 locus tags YY3DRAFT_04855 to 04860, respectively. From bottom to the top of each scaffold: Genes on forward strand (color by COG categories as denoted by the IMG platform), genes on reverse strand (color by COG categories), RNA genes (tRNAs green, sRNAs red, other RNAs black), GC content, GC skew

Table 4 Number of genes of Rhizobium mesoamericanum STM6155 associated with general COG functional categories

Insights from the genome sequence

R. mesoamericanum STM6155 shares 100 and 99% sequence identity (over 1346 bp) to the 16S rRNA of the fully sequenced R. mesoamericanum type strain CCGE501T [45] and R. mesoamericanum strain STM3625 [29], respectively. Moreover the STM6155 genome shows 96.18% average nucleotide identity (ANI) (with 82% of conserved DNA), with the type strain of R. mesoamericanum CCGE501T [20], fitting with the species affiliation cut-off defined by Goris et al. (2007) [46] (Table 5).

Table 5 Percentage of Average Nucleotide Identities (ANI)a among Rhizobium genomes

Extended insights

We produced plasmid profiles of several R. mesoamericanum isolates by the Eckhardt method [47] to compare their plasmid content with genomic data. As shown in Fig. 4, the STM6155 plasmid profile differs from those of STM3625 and CCGE501T. Firstly, the STM6155 and STM3629 plasmid profiles suggested the absence of a 1.5 Mbp megaplasmid (P1) observed in CCGE501T and STM3625. The alignment of the megaplasmid P1 sequence of STM3625 with the draft genomes of STM6155 and CCGE501T (Fig. 5a) using progressive Mauve software [48] shows, however, the presence of P1 homologous regions in STM6155 and CCGE501T genomes. This suggests a putative integration of megaplasmid P1 into the bacterial chromosome in STM6155. This phenomenon was already reported in cell siblings of Ensifer fredii (formerly Rhizobium sp.) NGR234 [49]. The STM6155 plasmid profile suggests thus a diversity of genome architectures at the intra-species level in R. mesoamericanum . This diversity is observed among isolates originating from different continents like STM6155 (New Caledonia) and STM3625 (French Guiana), but also among isolates from the same country like STM3625 and STM3629 (both from French Guiana) [15, 17]. Secondly, Fig. 4 shows that STM6155 harbors a ca. 500 Kbp symbiotic plasmid (pSym) of a slightly larger size than those of STM3625 and CCGE501T. The alignment of the STM3625 pSym with the draft genomes of STM6155 and CCGE501T (using progressive Mauve, Fig. 5b) confirms the observed pSym size difference, with the presence of additional genomic regions in the STM3625 pSym. Althabegoiti and colleagues [45] have previously observed that there is only 61.4% of conserved DNA (with ANI of 98.07%) between the pSyms of CCGE501T and STM3625. Here we can extend this observation to the STM6155 pSym, which differs from both STM3625 and CCGE501T pSyms.

Fig. 4
figure 4

Plasmid profiling of Rhizobium strains by the Eckhardt method. Plasmids were run on a 0.9% agarose gel at 5 Volts for 30 min then 60 Volts for 36h in a cold room. Lanes: 1: R. etli CFN42T (ladder); 2: R. tropici CIAT899T (ladder); 3: R. mesoamericanum STM3625 (French Guiana); 4: R. mesoamericanum STM3629 (French Guiana), 5: R. mesoamericanum STM6155 (New Caledonia); 6: R. mesoamericanum CCGE501T (Mexico). The * indicates the symbiotic plasmid

Fig. 5
figure 5

Alignments (using progressive Mauve software) of STM3625 megaplasmid P1 (A1) and pSym (B1) with draft genomes of R. mesoamericanum isolates STM6155 (A2, B2) and CCGE501T (A3, B3). The linked blocks in the alignment represent the common local colinear blocks (LCBs) among the compared genomes and homologous blocks among genomes are shown as identically colored regions. The red lines in A1 and B1 represent plasmid P1 boundaries (only P1 is shown), while in A2, B2, A3 and B3 they represent contigs boundaries (only homologous contigs to P1/pSym are shown)

Despite the sequence diversity of the pSyms within R. mesoamericanum isolates, the STM6155 symbiosis nodulation genes are highly conserved with those of STM3625 and CCGE501T. The STM6155 nodulation genes include nodA1BCSUIJHPQ, an additional nodA (nodA2) gene, three nodD (nodD1, 2 and 3) transcriptional regulator genes, nodM, and 2 nodO (nodO1, 2) genes. The gene order is also conserved in R. grahamii CCGE502T but this strain does not contain the nodA2 allele (Fig. 6).

Fig. 6
figure 6

Schematic organization of symbiotic genes conserved in Rhizobium mesoamericanum STM3625 and STM6155 and Rhizobium grahamii CCGE502T

Strain STM6155 was isolated from a nodule of M. pudica growing in ultramafic soil at a pH near neutral (pH 6.8) that contained high concentrations of heavy metals, and the highest concentrations of bioavailable chromate among four studied sites [15]. This strain was identified as being resistant to chromate concentrations up to 0.3 mM, that is comparable with chromate tolerance of Cupriavidus metallidurans CH34 [15, 50, 51]. Chromate resistance loci (chr) have been identified in the heavy-metal-tolerant C. metallidurans CH34 and we have discovered orthologs to these genes in STM6155 (Fig. 3c), that were absent from the more chromate sensitive strain R. mesoamericanum STM3625. MaGe [52] analysis has revealed synteny of six of the C. metallidurans CH34 plasmid-borne chr loci in STM6155. However, in contrast to CH3, the loci in STM6155 are arranged into two putative operons, chrBAP (locus tags YY3DRAFT_04858 - YY3DRAFT_04860) and chrCFY (locus tags YY3DRAFT_04857 - YY3DRAFT_04855) located adjacent to one another on complementary strands.

Conclusions

R. mesoamericanum STM6155 is a microsymbiont of Mimosa pudica L. and Phaseolus vulgaris L. [9], both of which have centres of origin in central/south America. The genome size of STM6155 is 6.9 Mbp with 58.9% GC content. This strain forms a clique with the two other R. mesoamericanum strains STM3625 and CCGE501T based on average nucleotide identity comparisons (species cut-off above 95% on >69% of conserved DNA, as defined by Goris et al. [46]. However, the genome of STM6155 has a different architecture compared with the genomes of STM3625 and CCGE501T, with STM6155 lacking a megaplasmid (P1) and containing a different sized pSym and small plasmid. Although STM6155 has a larger pSym, there is a notable symbiotic nod gene conservation between the three R. mesoamericanum strains, which is also shared with Rhizobium grahamii CCGE502T [20]. However, the genomes of the R. mesoamericanum strains contain two nodA alleles whereas R. grahamii CCGE502T genome has only one. Within the STM6155 genome, we have identified a chr chromate efflux gene cluster of six genes arranged into two putative operons and we postulate that this cluster is important for the survival of STM6155 in ultramafic soils containing high concentrations of chromate. The availability of sequenced genomes of R. mesoamericanum should provide further insights into rhizobial biogeographic distribution and should enable free-living and symbiotic attributes to be compared with those Mimosa symbioses induced by beta-rhizobia.

Abbreviations

½LA:

Half strength lupin agar

ANI:

Average nucleotide identity

GEBA-RNB:

Genomic encyclopedia for bacteria and Archaea-root nodule bacteria

IMG:

Integrated microbial genomes

TY:

Tryptone-yeast extract agar

References

  1. Simon MF, Grether R, de Queiroz LP, Särkinen TE, Dutra VF, Hughes CE. The evolutionary history of Mimosa (Leguminosae): toward a phylogeny of the sensitive plants. Am J Bot. 2011;98:1201–21.

    Article  PubMed  Google Scholar 

  2. Pacific Island Ecosystems at Risk (PIER) Mimosa pudica. http://www.hear.org/Pier/species/mimosa_pudica.htm. Accessed 21 Dec 2016.

  3. Ganaie SU, Abbasi T, Abbasi SA. Green synthesis of silver nanoparticles using an otherwise worthless weed Mimosa (Mimosa pudica): Feasibility and process development toward shape/size control. Particul Sci Technol. 2015;33:638–44.

    Article  CAS  Google Scholar 

  4. Ahmad H, Sehgal S, Mishra A, Gupta R. Mimosa pudica L. (Laajvanti): an overview. Pharmacogn Rev. 2012;6:115–25.

    Article  PubMed  PubMed Central  Google Scholar 

  5. Joseph B, George J, Mohan J. Pharmacology and traditional uses of Mimosa pudica. Int J Pharm Sci Drug Res. 2013;5:41–4.

    Google Scholar 

  6. Visoottiviseth P, Francesconi K, Sridokchan W. The potential of Thai indigenous plant species for the phytoremediation of arsenic contaminated land. Environ Pollut. 2002;118:453–61.

    Article  CAS  PubMed  Google Scholar 

  7. UNDP 2015. http://www.undp.org/content/undp/en/home/sdgoverview/post-2015-development-agenda.html. Accessed 21 Dec 2016.

  8. Moulin L, Munive A, Dreyfus B, Boivin-Masson C. Nodulation of legumes by members of the beta-subclass of Proteobacteria. Nature. 2001;411:948–50.

    Article  CAS  PubMed  Google Scholar 

  9. Gyaneshwar P, Hirsch AM, Moulin L, Chen WM, Elliott GN, Bontemps C, Estrada-de Los Santos P, Gross E, Dos Reis FB, Sprent JI, et al. Legume-nodulating betaproteobacteria: diversity, host range, and future prospects. Mol Plant Microb Interact. 2011;24:1276–88.

    Article  CAS  Google Scholar 

  10. Bournaud C, de Faria SM, Dos Santos JMF, Tisseyre P, Silva M, Chaintreuil C, Gross E, James EK, Prin Y, Moulin L. Burkholderia species are the most common and preferred nodulating symbionts of the Piptadenia group (tribe Mimoseae). PLoS One. 2013;8:e63478.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Beukes CW, Venter SN, Law IJ, Phalane FL, Steenkamp ET. South African papilionoid legumes are nodulated by diverse Burkholderia with unique nodulation and nitrogen-fixation loci. PLoS One. 2013;8:e68406.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Barrett CF, Parker MA. Coexistence of Burkholderia, Cupriavidus, and Rhizobium sp. nodule bacteria on two Mimosa spp. in Costa Rica. Appl Environ Microb. 2006;72:1198–206.

    Article  CAS  Google Scholar 

  13. Chen WM, Moulin L, Bontemps C, Vandamme P, Bena G, Boivin-Masson C. Legume symbiotic nitrogen fixation by beta-proteobacteria is widespread in nature. J Bacteriol. 2003;185:7266–672.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. dos Reis Jr FB, Simon MF, Gross E, Boddey RM, Elliott GN, Neto NE, de Fatima LM, de Queiroz LP, Scotti MR, Chen W-M, et al. Nodulation and nitrogen fixation by Mimosa spp. in the Cerrado and Caatinga biomes of Brazil. New Phytol. 2010;186:934–46.

    Article  Google Scholar 

  15. Klonowska A, Chaintreuil C, Tisseyre P, Miché L, Melkonian R, Ducousso M, Laguerre G, Brunel B, Moulin L. Biodiversity of Mimosa pudica rhizobial symbionts (Cupriavidus taiwanensis, Rhizobium mesoamericanum) in New Caledonia and their adaptation to heavy metal-rich soils. FEMS Microbiol Ecol. 2012;81:618–35.

    Article  CAS  PubMed  Google Scholar 

  16. Liu X, Wei S, Wang F, James EK, Guo X, Zagar C, Xia LG, Dong X, Wang YP. Burkholderia and Cupriavidus spp. are the preferred symbionts of Mimosa spp. in southern China. FEMS Microbiol Ecol. 2012;80:417–26.

    Article  CAS  PubMed  Google Scholar 

  17. Mishra RP, Tisseyre P, Melkonian R, Chaintreuil C, Miche L, Klonowska A, Gonzalez S, Bena G, Laguerre G, Moulin L. Genetic diversity of Mimosa pudica rhizobial symbionts in soils of French Guiana: investigating the origin and diversity of Burkholderia phymatum and other beta-rhizobia. FEMS Microbiol Ecol. 2012;79:487–503.

    Article  CAS  PubMed  Google Scholar 

  18. Elliott GN, Chou J-H, Chen W-M, Bloemberg GV, Bontemps C, Martínez-Romero E, Velázquez E, Young JPW, Sprent JI, James EK. Burkholderia spp. are the most competitive symbionts of Mimosa, particularly under N-limited conditions. Environ Microbiol. 2009;11:762–78.

    Article  PubMed  Google Scholar 

  19. Melkonian R, Moulin L, Béna G, Tisseyre P, Chaintreuil C, Heulin K, Rezkallah N, Klonowska A, Gonzalez S, Simon M, et al. The geographical patterns of symbiont diversity in the invasive legume Mimosa pudica can be explained by the competitiveness of its symbionts and by the host genotype. Environ Microbiol. 2014;16:2099–111.

    Article  PubMed  Google Scholar 

  20. López-López A, Rogel-Hernández M, Barois I, Ortiz Ceballos AI, Martínez J, Ormeño-Orrillo E, Martínez-Romero E. Rhizobium grahamii sp. nov. from Dalea leporina, Leucaena leucocephala, Clitoria ternatea nodules, and Rhizobium mesoamericanum sp. nov. from Phaseolus vulgaris, siratro, cowpea and Mimosa pudica nodules. Int J Syst Evol Microbiol. 2012;62:2264–71.

    Article  PubMed  Google Scholar 

  21. Bontemps C, Rogel MA, Wiechmann A, Mussabekova A, Moody S, Simon MF, Moulin L, Elliott GN, Lacercat-Didier L, Dasilva C, et al. Endemic Mimosa species from Mexico prefer alphaproteobacterial rhizobial symbionts. New Phytol. 2016;209:319–33.

    Article  CAS  PubMed  Google Scholar 

  22. Stopnisek N, Bodenhausen N, Frey B, Fierer N, Eberl L, Weisskopf L. Genus-wide acid tolerance accounts for the biogeographical distribution of soil Burkholderia populations. Environ Microbiol. 2014;16:1503–12.

    Article  CAS  PubMed  Google Scholar 

  23. Reeve WG, Ardley J, Tian R, Eshragi L, Yoon JW, Ngamwisetkun P, Seshadri R, Ivanova NN, Kyrpides NC. A genomic encyclopedia of the root nodule bacteria: assessing genetic diversity through a systematic biogeographic survey. Stand Genom Sci. 2015;10:14.

    Article  Google Scholar 

  24. Seshadri R, Reeve WG, Ardley JK, Tennessen K, Woyke T, Kyrpides NC, Ivanova NN. Discovery of novel plant interaction determinants from the genomes of 163 Root Nodule Bacteria. Sci Rep. 2015;5:16825.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Howieson JG, Ewing MA, D’Antuono MF. Selection for acid tolerance in Rhizobium meliloti. Plant Soil. 1988;105:179–88.

    Article  CAS  Google Scholar 

  26. Beringer JE. R factor transfer in Rhizobium leguminosarum. J Gen Microbiol. 1974;84:188–98.

    CAS  PubMed  Google Scholar 

  27. Vincent JM. A manual for the practical study of the root-nodule bacteria. International Biological Programme. Oxford: Blackwell Scientific Publications; 1970.

    Google Scholar 

  28. Kim O, Cho Y, Lee K, Yoon S, Kim M, Na H, Park S, Jeon Y, Lee J, Yi H, et al. Introducing EzTaxon-e: a prokaryotic 16S rRNA gene sequence database with phylotypes that represent uncultured species. Int J Syst Evol Microbiol. 2012;62:716–21.

    Article  CAS  PubMed  Google Scholar 

  29. Moulin L, Mornico D, Melkonian R, Klonowska A. Draft genome sequence of Rhizobium mesoamericanum STM3625, a nitrogen-fixing symbiont of Mimosa pudica isolated in French Guiana (South America). Genome Announc. 2013;1:e00066–00012.

    Article  PubMed  PubMed Central  Google Scholar 

  30. Reddy TBK, Thomas AD, Stamatis D, Bertsch J, Isbandi M, Jansson J, Mallajosyula J, Pagani I, Lobos EA, Kyrpides NC. The Genomes OnLine Database (GOLD) v.5: a metadata management system based on a four level (meta)genome project classification. Nucleic Acids Res. 2015;43:D1099–106.

  31. Markowitz VM, Chen IA, Palaniappan K, Chu K, Szeto E, Pillay M, Ratner A, Huang J, Woyke T, Huntemann M, et al. IMG 4 version of the integrated microbial genomes comparative analysis system. Nucleic Acids Res. 2014;42:D560–67.

    Article  CAS  PubMed  Google Scholar 

  32. Joint Genome Institute Protocols. http://jgi.doe.gov/user-program-info/pmo-overview/protocols-sample-preparation-information/. Accessed 21 Dec 2016.

  33. Bennett S. Solexa Ltd. Pharmacogenomics. 2004;5:433–38.

    Article  PubMed  Google Scholar 

  34. Joint Genome Institute. http://jgi.doe.gov/. Accessed 21 Dec 2016.

  35. Zerbino DR. Using the velvet de novo assembler for short-read sequencing technologies. Curr Protoc Bioinformatics. 2010;11(11):15.

    Google Scholar 

  36. GitHub - lh3/wgsim: Reads simulator. https://github.com/lh3/wgsim. Accessed 21 Dec 2016.

  37. Gnerre S, MacCallum I, Przybylski D, Ribeiro FJ, Burton JN, Walker BJ, Sharpe T, Hall G, Shea TP, Sykes S, et al. High-quality draft assemblies of mammalian genomes from massively parallel sequence data. Proc Natl Acad Sci U S A. 2011;108:1513–518.

    Article  CAS  PubMed  Google Scholar 

  38. Hyatt D, Chen GL, Locascio PF, Land ML, Larimer FW, Hauser LJ. Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Bioinform. 2010;11:119.

    Article  Google Scholar 

  39. Chen IMA, Markowitz VM, Chu K, Anderson I, Mavromatis K, Kyrpides NC, Ivanova NN. Improving microbial genome annotations in an integrated database context. PLoS One. 2013;8:e54859.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Huntemann M, Ivanova NN, Mavromatis K, Tripp HJ, Paez-Espino D, Palaniappan K, Szeto E, Pillay M, Chen IM-A, Pati A, et al. The standard operating procedure of the DOE-JGI microbial genome annotation pipeline (MGAP v.4). Stand Genom Sci. 2015;10:86.

  41. Lowe TM, Eddy SR. tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res. 1997;25:955–64.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Pruesse E, Quast C, Knittel K, Fuchs BM, Ludwig W, Peplies J, Glöckner FO. SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Res. 2007;35:7188–196.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Nawrocki EP, Eddy SR. Infernal 1.1: 100-fold faster RNA homology searches. Bioinformatics. 2013;29:2933–935.

  44. Markowitz VM, Mavromatis K, Ivanova NN, Chen IM, Chu K, Kyrpides NC. IMG ER: a system for microbial genome annotation expert review and curation. Bioinformatics. 2009;25:2271–78.

    Article  CAS  PubMed  Google Scholar 

  45. Althabegoiti MJ, Ormeño-Orrillo E, Lozano L, Torres Tejerizo G, Rogel MA, Mora J, Martínez-Romero E. Characterization of Rhizobium grahamii extrachromosomal replicons and their transfer among rhizobia. BMC Microbiol. 2014;14:6.

    Article  PubMed  PubMed Central  Google Scholar 

  46. Goris J, Konstantinidis KT, Klappenbach J, Coenye T, Vandamme P, Tiedje JM. DNA-DNA hybridization values and their relationship to whole-genome sequence similarities. Int J Syst Evol Microbiol. 2007;57:81–91.

    Article  CAS  PubMed  Google Scholar 

  47. Eckhardt T. A rapid method for the identification of plasmid deoxyribonucleic acid in bacteria. Plasmid. 1978;1:584–88.

    Article  CAS  PubMed  Google Scholar 

  48. Darling AE, Mau B, Perna NT. progressiveMauve: multiple genome alignment with gene gain, loss and rearrangement. PLoS One. 2010;5:e11147.

    Article  PubMed  PubMed Central  Google Scholar 

  49. Mavingui P, Flores M, Guo X, Dávila G, Perret X, Broughton WJ, Palacios R. Dynamics of genome architecture in Rhizobium sp. strain NGR234. J Bacteriol. 2002;184:171–76.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Janssen PJ, Van Houdt R, Moors H, Monsieurs P, Morin N, Michaux A, Benotmane MA, Leys N, Vallaeys T, Lapidus A, et al. The complete genome sequence of Cupriavidus metallidurans strain CH34, a master survivalist in harsh and anthropogenic environments. PLoS One. 2010;5:e10433.

    Article  PubMed  PubMed Central  Google Scholar 

  51. Juhnke S, Peitzsch N, Hübener N, Große C, Nies DH. New genes involved in chromate resistance in Ralstonia metallidurans strain CH34. Arch Microbiol. 2002;179:15–25.

    Article  CAS  PubMed  Google Scholar 

  52. Vallenet D, Labarre L, Rouy Z, Barbe V, Bocs S, Cruveiller S, Lajus A, Pascal G, Scarpelli C, Medigue C. MaGe: a microbial genome annotation system supported by synteny results. Nucleic Acids Res. 2006;34:53–65.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol. 2011;28:2731–739.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Nei M, Kumar S. Molecular evolution and phylogenetics. New York: Oxford University Press; 2000.

    Google Scholar 

  55. Felsenstein J. Confidence limits on phylogenies: an approach using the bootstrap. Evolution. 1985;39:783–91.

    Article  Google Scholar 

  56. Field D, Garrity G, Gray T, Morrison N, Selengut J, Sterk P, Tatusova T, Thomson N, Allen M, Angiuoli SV, et al. Towards a richer description of our complete collection of genomes and metagenomes “minimum information about a genome sequence” (MIGS) specification. Nat Biotechnol. 2008;26:541–7.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Field D, Amaral-Zettler L, Cochrane G, Cole JR, Dawyndt P, Garrity GM, Gilbert J, Glöckner FO, Hirschman L, Karsch-Mizrachi I, et al. The genomic standards consortium. PLoS Biol. 2011;9:e1001088.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Woese CR, Kandler O, Wheelis ML. Towards a natural system of organisms: proposal for the domains archaea, bacteria, and eucarya. Proc Natl Acad Sci U S A. 1990;87:4576–579.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Editor L. Validation of publication of new names and new combinations previously effectively published outside the IJSEM. IntJ Syst Evol Micr. 2005;55:2235–238.

    Article  Google Scholar 

  60. Chen WX, Wang ET, Kuykendall LD. The Proteobacteria. New York: Springer - Verlag; 2005.

    Google Scholar 

  61. Garrity GM, Bell JA, Lilburn T: Class I. Alphaproteobacteria class. In: Garrity GM, Brenner DJ, Kreig NR, Staley JT, editors. Bergey’s manual of systematic bacteriology. 2nd ed. New York: Springer - Verlag; 2005.

    Google Scholar 

  62. Kuykendall LD. Order VI. Rhizobiales ord. nov. In: Garrity GM, Brenner DJ, Kreig NR, Staley JT, editors. Bergey’s manual of systematic bacteriology. 2nd ed. New York: Springer - Verlag; 2005. p. 324.

    Google Scholar 

  63. Kuykendall LD. Family I. Rhizobiaceae. In: Garrity GM, Brenner DJ, Krieg NR, Staley JT, editors. Bergey’s manual of systematic bacteriology. New York: Springer - Verlag; 2005.

    Google Scholar 

  64. Biological Agents: Technical rules for biological agents. http://www.baua.de/en/Topics-from-A-to-Z/Biological-Agents/TRBA/TRBA.html. Accessed 21 Dec 2016.

  65. Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, Davis AP, Dolinski K, Dwight SS, Eppig JT, et al. Gene ontology: tool for the unification of biology. The gene ontology consortium. Nat Genet. 2000;25:25–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Guide to GO Evidence Codes. http://geneontology.org/page/guide-go-evidence-codes. Accessed 21 Dec 2016.

  67. Rhizobium mesoamericanum STM6155 Genome sequencing and assembly. http://www.ncbi.nlm.nih.gov/bioproject/?term=YY3. Accessed 21 Dec 2016.

  68. Richter M, Rosselló-Móra R. Shifting the genomic gold standard for the prokaryotic species definition. Proc Natl Acad Sci U S A. 2009;106:19126–131.

Download references

Acknowledgements

We thank Gordon Thompson (Murdoch University) for the preparation of SEM and TEM photos.

Funding

This work was performed under the auspices of the US Department of Energy’s Office of Science, Biological and Environmental Research Program, and by the University of California, Lawrence Berkeley National Laboratory under contract No. DE-AC02-05CH11231. We gratefully acknowledge the funding received from the French National Agency of Research (Project BETASYM ANR-09-JCJ-0046), Curtin University Sustainability Policy Institute, and the funding received from Murdoch University Small Research Grants Scheme in 2016.

Authors’ contributions

LM supplied the strain, AK and LM the background information for this project and AK, JA, LM, TR and WR drafted the manuscript. TR provided the DNA to the JGI and performed all imaging, MB and NB provided financial support and ALL, MG, DM, MH, TBKR, NV, TW, VM, NI, RS and NK were involved in sequencing the genome and/or editing the final paper. All authors read and approved the final manuscript.

Competing interests

The authors declare that they have no competing interests.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Wayne Reeve.

Additional file

Additional file 1: Table S1.

Associated MIGS record for STM6155. Table S2. Nodulation and N2 fixation properties of Rhizobium mesoamericanum STM6155 on selected legume hosts. (DOCX 50 kb)

Rights and permissions

Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Klonowska, A., López-López, A., Moulin, L. et al. High-quality draft genome sequence of Rhizobium mesoamericanum strain STM6155, a Mimosa pudica microsymbiont from New Caledonia. Stand in Genomic Sci 12, 7 (2017). https://doi.org/10.1186/s40793-016-0212-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1186/s40793-016-0212-4

Keywords