Whole Genome Analyses Suggests that Burkholderia sensu lato Contains Two Additional Novel Genera (Mycetohabitans gen. nov., and Trinickia gen. nov.): Implications for the Evolution of Diazotrophy and Nodulation in the Burkholderiaceae

Santos, Paulina Estrada‐de los; Palmer, Marike; Chávez-Ramírez, Belén; Beukes, Chrizelle W.; Steenkamp, Emma Theodora; Briscoe, Leah; Khan, Noor; Maluk, Marta; Lafos, Marcel; Humm, Ethan A.; Arrabit, Monique; Crook, Martin F.; Gross, Eduardo; Simon, Marcelo F.; Reis, Fábio Bueno dos; Whitman, William B.; Shapiro, Nicole; Poole, Philip S.; Hirsch, Ann M.; Venter, Stephanus N.; James, Euan K.

doi:10.3390/genes9080389

Cited by 218 publications

(169 citation statements)

References 75 publications

(114 reference statements)

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“…Our inferred species tree of BCC reconstructed by these markers provided us with an accurate phylogenetic relationship. Together with dDDH and ANI, two methods that are useful for species demarcation and are powerful in BCC species differentiation [1,64,65], we delineated BCC species as 36 clusters. The results showed that the 22 currently known species correspond to 22 of these clusters (Fig.…”

Section: Discussionmentioning

confidence: 99%

Genome-based classification of Burkholderia cepacia complex provides new insight into its taxonomic status

Yuan¹,

Zhou²,

Zhou³

et al. 2020

Biol Direct

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Background: Accurate classification of different Burkholderia cepacia complex (BCC) species is essential for therapy, prognosis assessment and research. The taxonomic status of BCC remains problematic and an improved knowledge about the classification of BCC is in particular needed. Methods: We compared phylogenetic trees of BCC based on 16S rRNA, recA, hisA and MLSA (multilocus sequence analysis). Using the available whole genome sequences of BCC, we inferred a species tree based on estimated single-copy orthologous genes and demarcated species of BCC using dDDH/ANI clustering. Results: We showed that 16S rRNA, recA, hisA and MLSA have limited resolutions in the taxonomic study of closely related bacteria such as BCC. Our estimated species tree and dDDH/ANI clustering clearly separated 116 BCC strains into 36 clusters. With the appropriate reclassification of misidentified strains, these clusters corresponded to 22 known species as well as 14 putative novel species. Conclusions: This is the first large-scale and systematic study of the taxonomic status of the BCC and could contribute to further insights into BCC taxonomy. Our study suggested that conjunctive use of core phylogeny based on single-copy orthologous genes, as well as pangenome-based dDDH/ANI clustering would provide a preferable framework for demarcating closely related species. Reviewer: This article was reviewed by Dr. Xianwen Ren.

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Section: Discussionmentioning

confidence: 99%

Genome-based classification of Burkholderia cepacia complex provides new insight into its taxonomic status

Yuan¹,

Zhou²,

Zhou³

et al. 2020

Biol Direct

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“…Recently, diverse bacterial-fungal symbioses have been described, with fungal hosts ranging from tree endophytes to human pathogens (Arora and Riyaz-Ul-Hassan, 2018). One such partnership is Mycetohabitans rhizoxinica (family Burkholderiaceae; formerly Burkholderia rhizoxinica (Estrada-de Los Santos et al, 2018)) and the mucoromycete Rhizopus microsporus. A rice pathogen and opportunistic human pathogen, R. microsporus can also be found as a free-living soil saprophyte and is used in soy fermentation.…”

Section: Introductionmentioning

confidence: 99%

“…Despite the demonstrated importance of the T3SS in the Rhizopus-Mycetohabitans partnership, no T3 effector proteins from M. rhizoxinica or any other endohyphal bacterium have been characterized (Nazir et al, 2017). However, homologs of transcription activator-like (TAL) effectors from plant pathogenic bacteria were identified in the first sequenced M. rhizoxinica genome (Lackner et al, 2011b;de Lange et al, 2014b;Juillerat et al, 2014;Estrada-de Los Santos et al, 2018). TAL effectors are T3secreted, sequence-specific, DNA-binding proteins that act as transcription factors once inside plant cells, upregulating target genes.…”

Section: Introductionmentioning

confidence: 99%

A TAL effector-like protein of symbioticMycetohabitansincreases stress tolerance and alters the transcriptome of the fungal hostRhizopus microsporus

Carter

Carpenter

Dubrow

et al. 2020

Preprint

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Symbioses of bacteria with fungi have only recently been described and are poorly understood. In the symbiosis of Mycetohabitans (formerly Burkholderia) rhizoxinica with the fungus Rhizopus microsporus, bacterial type III (T3) secretion is known to be essential. Proteins resembling T3-secreted transcription activator-like (TAL) effectors of plant pathogenic bacteria are encoded in the three sequenced Mycetohabitans spp. genomes. TAL effectors nuclear localize in plants, where they bind and activate genes important in disease. The Burkholderia TAL-like (Btl) proteins bind DNA but lack the Nand C-terminal regions in which TAL effectors harbor their T3 and nuclear localization signals, and activation domain. We characterized a Btl protein, Btl19-13, and found that, despite the structural differences, it can be T3-secreted and can nuclear localize. A btl19-13 gene knockout did not prevent the bacterium from infecting the fungus, but the fungus became less tolerant to cell membrane stress. Btl19-13 did not alter transcription in a plant-based reporter assay, but 15 R. microsporus genes were differentially expressed in comparisons both of the fungus infected with the wildtype bacterium vs the mutant and with the mutant vs. a complemented strain. Southern blotting revealed btl genes in 14 diverse Mycetohabitans isolates. However, banding patterns and available sequences suggest variation, and the btl19-13 phenotype could not be rescued by a btl gene from a different strain. Our findings support the conclusion that Btl proteins are effectors that act on host DNA and play important but varied or possibly host-genotype-specific roles in the M. rhizoxinica-R. microsporus symbiosis.

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“…The majority of bacteria that fix nitrogen in root nodules of leguminous plants are members of the α-Proteobacteria, Rhizobium, Bradyrhizobium, Ensifer , Phyllobacterium , Mesorhizobium , Devosia , Azorhizobium , Allorhizobium (Hirsch 1992; Sawada et al 2003; Lafay and Burdon 2007) and also Microvirga (Ardley et al 2012). Among the β-Proteobacteria, members of the Burkholderiaceae , known as beta-rhizobia, also nodulate legumes (Bontemps et al 2010, Gyaneshwar et al 2011, Estrada de los Santos et al 2018).…”

Section: Introductionmentioning

confidence: 99%

“…Most of the NRE are not pathogenic, but some may be serious pathogens of animals or plants, e.g., Staphylococcus, Bordetella (Sturz et al 1997; Xu et al 2014) and species of Burkholderiaceae such as B. cepacia (Eberl and Vandamme 2016). In the last few years, many of the symbiotic Burkholderia species (Gyaneshwar et al 2011) have been placed into new genera, e.g., Paraburkholderia and Trinickia (Sawana et al 2014; Estrada de los Santos et al 2018).…”

Section: Introductionmentioning

confidence: 99%

Impact of soil salinity on the cowpea nodule-microbiome and the isolation of halotolerant PGPR strains to promote plant growth under salinity stress

Mukhtar

Hirsch²,

Khan

et al. 2019

Preprint

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Four soil samples (SS-1-SS-4) isolated from semi-arid soils in Punjab, Pakistan were used as inocula for cowpea (Vigna unguiculata L.) grown under salinity stress to analyze the composition of bacteria in the rhizosphere and within nodules through cultivation-dependent and cultivationindependent methods. Two cowpea varieties, 603 and the salt-tolerant CB 46, were each inoculated with four different native soil samples, and data showed that plants inoculated with soil samples SS-2 and SS-4 grew better than plants inoculated with soil samples SS-1 and SS-3. Bacteria were isolated from both soils and nodules, and 34 of the 51 original isolates tested positive for PGPR traits in plate assays with many exhibiting multiple plant growth-promoting properties. A number of isolates were positive for all PGPR traits tested. For the microbiome studies, environmental DNA (eDNA) was isolated from SS-1 and SS-4, which represented the extremes of the Pakistan soils to which the plants responded, and by 16S rRNA gene sequencing analysis were found to consist mainly of Actinobacteria, Firmicutes, and Proteobacteria. However, sequencing analysis of eDNA isolated from cowpea nodules established by the trap plants grown in the four Pakistan soils indicated that the nodule microbiome consisted almost exclusively of Proteobacterial sequences, particularly Bradyrhizobium. Yet, many other bacteria including Rhizobium, Mesorhizobium, Pseudomonas, as well as Paenibacillus, Bacillus as well as non-proteobacterial genera were isolated from the nodules of soil-inoculated cowpea plants. This discrepancy between the bacteria isolated from cowpea nodules (Proteobacteria and non-Proteobacteria) versus those detected in the nodule microbiome (Proteobacteria) needs further study.

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Whole Genome Analyses Suggests that Burkholderia sensu lato Contains Two Additional Novel Genera (Mycetohabitans gen. nov., and Trinickia gen. nov.): Implications for the Evolution of Diazotrophy and Nodulation in the Burkholderiaceae

Cited by 218 publications

References 75 publications

Genome-based classification of Burkholderia cepacia complex provides new insight into its taxonomic status

Genome-based classification of Burkholderia cepacia complex provides new insight into its taxonomic status

A TAL effector-like protein of symbioticMycetohabitansincreases stress tolerance and alters the transcriptome of the fungal hostRhizopus microsporus

Impact of soil salinity on the cowpea nodule-microbiome and the isolation of halotolerant PGPR strains to promote plant growth under salinity stress

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