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A novel taxonomic marker that discriminates between morphologically complex actinomycetes.

Girard G, Traag BA, Sangal V, Mascini N, Hoskisson PA, Goodfellow M, van Wezel GP - Open Biol (2013)

Bottom Line: The almost complete conservation of the SsgB amino acid (aa) sequence between members of the same genus and its high divergence between even closely related genera provides high-quality data for the classification of morphologically complex actinomycetes.Our analysis validates Kitasatospora as a sister genus to Streptomyces in the family Streptomycetaceae and suggests that Micromonospora, Salinispora and Verrucosispora may represent different clades of the same genus.It is also apparent that the aa sequence of SsgA is an accurate determinant for the ability of streptomycetes to produce submerged spores, dividing the phylogenetic tree of streptomycetes into liquid-culture sporulation and no liquid-culture sporulation branches.

View Article: PubMed Central - PubMed

Affiliation: Molecular Biotechnology, Institute of Biology, Leiden University, PO Box 9505, 2300 RA Leiden, The Netherlands.

ABSTRACT
In the era when large whole genome bacterial datasets are generated routinely, rapid and accurate molecular systematics is becoming increasingly important. However, 16S ribosomal RNA sequencing does not always offer sufficient resolution to discriminate between closely related genera. The SsgA-like proteins are developmental regulatory proteins in sporulating actinomycetes, whereby SsgB actively recruits FtsZ during sporulation-specific cell division. Here, we present a novel method to classify actinomycetes, based on the extraordinary way the SsgA and SsgB proteins are conserved. The almost complete conservation of the SsgB amino acid (aa) sequence between members of the same genus and its high divergence between even closely related genera provides high-quality data for the classification of morphologically complex actinomycetes. Our analysis validates Kitasatospora as a sister genus to Streptomyces in the family Streptomycetaceae and suggests that Micromonospora, Salinispora and Verrucosispora may represent different clades of the same genus. It is also apparent that the aa sequence of SsgA is an accurate determinant for the ability of streptomycetes to produce submerged spores, dividing the phylogenetic tree of streptomycetes into liquid-culture sporulation and no liquid-culture sporulation branches. A new phylogenetic tree of industrially relevant actinomycetes is presented and compared with that based on 16S rRNA sequences.

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Alignment of SsgA orthologues. Only those SsgA protein sequences have been used as input that are derived from species with known phenotype in submerged cultures. For shading, at least 60% of the aligned proteins should share the same or similar aa residues. Identical residues shaded black, similar residues shaded grey. Residues highlighted with an asterisk above the alignment, are conserved within—but different between—the ‘LSp’ and ‘NLSp’ branches in figure 5 and function as identifiers for the ability of a certain Streptomyces species to sporulate in submerged culture. Sequences were labelled by their strain of origin, for sequence labels see §4.2. For input sequences and their accession numbers, see the electronic supplementary material, data file S4.
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RSOB130073F4: Alignment of SsgA orthologues. Only those SsgA protein sequences have been used as input that are derived from species with known phenotype in submerged cultures. For shading, at least 60% of the aligned proteins should share the same or similar aa residues. Identical residues shaded black, similar residues shaded grey. Residues highlighted with an asterisk above the alignment, are conserved within—but different between—the ‘LSp’ and ‘NLSp’ branches in figure 5 and function as identifiers for the ability of a certain Streptomyces species to sporulate in submerged culture. Sequences were labelled by their strain of origin, for sequence labels see §4.2. For input sequences and their accession numbers, see the electronic supplementary material, data file S4.

Mentions: SsgA proteins from different streptomycetes generally share between 75% and 90% end-to-end sequence identity, with few differences between the N-termini, and regions with higher variability in the core (approx. residues 53–92 of S. coelicolor SsgA) and the C-termini (approx. beyond residue 110) of the proteins (figure 4). SsgA from Streptomyces clavuligerus ATCC 27064T is the most distinct of all sequenced orthologues, with a sequence identity to other orthologues varying from 63% (compared with Streptomyces collinus and Streptomyces ramocissimus SsgA) to 73% (compared with S. venezuelae SsgA). SsgA proteins from S. coelicolor and Streptomyces lividans TK24 are identical, whereas their genes contain a single nucleotide difference (His42 encoded by CAT in S. coelicolor and by CAC in S. lividans). More notably, the predicted SsgA orthologues from S. griseus and S. roseosporus are also identical, whereas 17 ‘silent’ nucleotide differences occur between their respective DNA sequences, suggesting evolutionary pressure to maintain the aa sequence.Figure 4.


A novel taxonomic marker that discriminates between morphologically complex actinomycetes.

Girard G, Traag BA, Sangal V, Mascini N, Hoskisson PA, Goodfellow M, van Wezel GP - Open Biol (2013)

Alignment of SsgA orthologues. Only those SsgA protein sequences have been used as input that are derived from species with known phenotype in submerged cultures. For shading, at least 60% of the aligned proteins should share the same or similar aa residues. Identical residues shaded black, similar residues shaded grey. Residues highlighted with an asterisk above the alignment, are conserved within—but different between—the ‘LSp’ and ‘NLSp’ branches in figure 5 and function as identifiers for the ability of a certain Streptomyces species to sporulate in submerged culture. Sequences were labelled by their strain of origin, for sequence labels see §4.2. For input sequences and their accession numbers, see the electronic supplementary material, data file S4.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3814722&req=5

RSOB130073F4: Alignment of SsgA orthologues. Only those SsgA protein sequences have been used as input that are derived from species with known phenotype in submerged cultures. For shading, at least 60% of the aligned proteins should share the same or similar aa residues. Identical residues shaded black, similar residues shaded grey. Residues highlighted with an asterisk above the alignment, are conserved within—but different between—the ‘LSp’ and ‘NLSp’ branches in figure 5 and function as identifiers for the ability of a certain Streptomyces species to sporulate in submerged culture. Sequences were labelled by their strain of origin, for sequence labels see §4.2. For input sequences and their accession numbers, see the electronic supplementary material, data file S4.
Mentions: SsgA proteins from different streptomycetes generally share between 75% and 90% end-to-end sequence identity, with few differences between the N-termini, and regions with higher variability in the core (approx. residues 53–92 of S. coelicolor SsgA) and the C-termini (approx. beyond residue 110) of the proteins (figure 4). SsgA from Streptomyces clavuligerus ATCC 27064T is the most distinct of all sequenced orthologues, with a sequence identity to other orthologues varying from 63% (compared with Streptomyces collinus and Streptomyces ramocissimus SsgA) to 73% (compared with S. venezuelae SsgA). SsgA proteins from S. coelicolor and Streptomyces lividans TK24 are identical, whereas their genes contain a single nucleotide difference (His42 encoded by CAT in S. coelicolor and by CAC in S. lividans). More notably, the predicted SsgA orthologues from S. griseus and S. roseosporus are also identical, whereas 17 ‘silent’ nucleotide differences occur between their respective DNA sequences, suggesting evolutionary pressure to maintain the aa sequence.Figure 4.

Bottom Line: The almost complete conservation of the SsgB amino acid (aa) sequence between members of the same genus and its high divergence between even closely related genera provides high-quality data for the classification of morphologically complex actinomycetes.Our analysis validates Kitasatospora as a sister genus to Streptomyces in the family Streptomycetaceae and suggests that Micromonospora, Salinispora and Verrucosispora may represent different clades of the same genus.It is also apparent that the aa sequence of SsgA is an accurate determinant for the ability of streptomycetes to produce submerged spores, dividing the phylogenetic tree of streptomycetes into liquid-culture sporulation and no liquid-culture sporulation branches.

View Article: PubMed Central - PubMed

Affiliation: Molecular Biotechnology, Institute of Biology, Leiden University, PO Box 9505, 2300 RA Leiden, The Netherlands.

ABSTRACT
In the era when large whole genome bacterial datasets are generated routinely, rapid and accurate molecular systematics is becoming increasingly important. However, 16S ribosomal RNA sequencing does not always offer sufficient resolution to discriminate between closely related genera. The SsgA-like proteins are developmental regulatory proteins in sporulating actinomycetes, whereby SsgB actively recruits FtsZ during sporulation-specific cell division. Here, we present a novel method to classify actinomycetes, based on the extraordinary way the SsgA and SsgB proteins are conserved. The almost complete conservation of the SsgB amino acid (aa) sequence between members of the same genus and its high divergence between even closely related genera provides high-quality data for the classification of morphologically complex actinomycetes. Our analysis validates Kitasatospora as a sister genus to Streptomyces in the family Streptomycetaceae and suggests that Micromonospora, Salinispora and Verrucosispora may represent different clades of the same genus. It is also apparent that the aa sequence of SsgA is an accurate determinant for the ability of streptomycetes to produce submerged spores, dividing the phylogenetic tree of streptomycetes into liquid-culture sporulation and no liquid-culture sporulation branches. A new phylogenetic tree of industrially relevant actinomycetes is presented and compared with that based on 16S rRNA sequences.

Show MeSH
Related in: MedlinePlus