Taxonomic evaluation of the Streptomyces hygroscopicus clade using multilocus sequence analysis and DNA–DNA hybridization, validating the MLSA scheme for systematics of the whole genus

Rong, Xiaoying; Huang, Ying

doi:10.1016/j.syapm.2011.10.004

Cited by 174 publications

(181 citation statements)

References 39 publications

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“…gyrB displayed the widest distance range, and atpD had the highest nucleotide diversity, while rpoB showed both the narrowest distance range and lowest nucleotide diversity. The concatenated alignment of the five loci showed that MLSA distances between the strains ranged from 0 to 0.006 (mean, 0.003), values below the 0.007 cutoff point recommended for the delineation of genomic species of Streptomyces (25,26). Regarding alleles, many were observed more than once, and the ones most frequently found were atpD1, gyrB2, recA1, rpoB1, and trpB5, observed 12, 20, 18, 23, and 14 times, respectively ( Table 1).…”

Section: Resultsmentioning

confidence: 94%

“…Our previously established streptomycete MLSA scheme (24), relying on five housekeeping genes, atpD (ATP synthase F1, ␤ subunit), gyrB (DNA gyrase, B subunit), recA (recombinase A), rpoB (RNA polymerase, ␤ subunit), and trpB (tryptophan synthase, ␤ subunit), has been successfully applied to systematic analyses of four Streptomyces 16S rRNA gene clades at inter-and intraspecies levels (17,22,(24)(25)(26) and has also shown great potential in population genetics analysis of streptomycetes (18). In the present study, a collection of 41 S. albidoflavus strains from diverse sources was subjected to the five-gene-based MLSA scheme to describe the population structure of S. albidoflavus, followed by various analyses to examine the roles homologous recombination and habitat played in shaping such structure.…”

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confidence: 99%

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Population Genetic Analysis of Streptomyces albidoflavus Reveals Habitat Barriers to Homologous Recombination in the Diversification of Streptomycetes

Cheng

Rong

Pinto‐Tomás

et al. 2015

Appl Environ Microbiol

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Examining the population structure and the influence of recombination and ecology on microbial populations makes great sense for understanding microbial evolution and speciation. Streptomycetes are a diverse group of bacteria that are widely distributed in nature and a rich source of useful bioactive compounds; however, they are rarely subjected to population genetic investigations. In this study, we applied a five-gene-based multilocus sequence analysis (MLSA) scheme to 41 strains of Streptomyces albidoflavus derived from diverse sources, mainly insects, sea, and soil. Frequent recombination was detected in S. albidoflavus, supported by multiple lines of evidence from the pairwise homoplasy index (⌽ w ) test, phylogenetic discordance, the Shimodaira-Hasegawa (SH) test, and network analysis, underpinning the predominance of homologous recombination within Streptomyces species. A strong habitat signal was also observed in both phylogenetic and Structure 2.3.3 analyses, indicating the importance of ecological difference in shaping the population structure. Moreover, all three habitat-associated groups, particularly the entomic group, demonstrated significantly reduced levels of gene flow with one another, generally revealing habitat barriers to recombination. Therefore, a combined effect of homologous recombination and ecology is inferred for S. albidoflavus, where dynamic evolution is at least partly balanced by the extent that differential distributions of strains among habitats limit genetic exchange. Our study stresses the significance of ecology in microbial speciation and reveals the coexistence of homologous recombination and ecological divergence in the evolution of streptomycetes. Despite various currently available approaches to defining prokaryotic species and a growing recognition of their vast diversity in nature, the concept of microbial species has long been under dispute due to their widespread genomic heterogeneity and variable levels of gene exchange (1-3). Genetic clusters that emerge in molecular sequence analyses of populations are often regarded as bearing the status of species, and multiple theoretical models to resolve the evolutionary mechanisms that cause the creation and maintenance of the genetic clusters have been proposed (3, 4). Until now, two major parallel concepts of microbial species have been developed, focused on barriers to recombination and ecological divergence, respectively (4): the neutral model, raised by Fraser and colleagues (3, 5), highlights the role of recombination in converging and diverging clusters with various recombination rates, while the ecotype model, developed by Cohan and colleagues (6, 7), defines an ecotype as a group of ecologically similar strains which is purged of its diversity by periodic selection and/or genetic drift. Consequently, recombination and divergent selection have emerged as two key processes driving the increasing discussion concerning theoretical models of microbial speciation. Moreover, coexistence of these processes has been suggeste...

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Section: Resultsmentioning

confidence: 94%

mentioning

confidence: 99%

Population Genetic Analysis of Streptomyces albidoflavus Reveals Habitat Barriers to Homologous Recombination in the Diversification of Streptomycetes

Cheng

Rong

Pinto‐Tomás

et al. 2015

Appl Environ Microbiol

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“…The taxonomy of Streptomyces species is particularly challenging due to the high number of species and the limited resolution of the 16S rRNA gene for species circumscription (32). This has led to the adoption of multilocus sequence analysis approaches to resolve the taxonomy of this genus (33)(34)(35). Using a five-gene phylogeny, 31 of the 32 total Streptomyces isolates were placed in 21 different species, including 15 novel clades ( Table 2 and Fig.…”

Section: Resultsmentioning

confidence: 99%

“…All analyses were subjected to 500 bootstrap replicates. Multilocus sequence analysis (MLSA) evolutionary distances were determined using MEGA6 by calculating the Kimura 2-parameter distance (70), and strain pairs having distance less than 0.007 were considered conspecific based on the guideline empirically determined by Rong and Huang (34).…”

Section: Methodsmentioning

confidence: 99%

Western Bats as a Reservoir of Novel Streptomyces Species with Antifungal Activity

Hamm

Caimi

Northup

et al. 2017

Appl Environ Microbiol

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At least two-thirds of commercial antibiotics today are derived from Actinobacteria, more specifically from the genus Streptomyces. Antibiotic resistance and new emerging diseases pose great challenges in the field of microbiology. Cave systems, in which actinobacteria are ubiquitous and abundant, represent new opportunities for the discovery of novel bacterial species and the study of their interactions with emergent pathogens. White-nose syndrome is an invasive bat disease caused by the fungus Pseudogymnoascus destructans, which has killed more than six million bats in the last 7 years. In this study, we isolated naturally occurring actinobacteria from white-nose syndrome (WNS)-free bats from five cave systems and surface locations in the vicinity in New Mexico and Arizona, USA. We sequenced the 16S rRNA region and tested 632 isolates from 12 different bat species using a bilayer plate method to evaluate antifungal activity. Thirty-six actinobacteria inhibited or stopped the growth of P. destructans, with 32 (88.9%) actinobacteria belonging to the genus Streptomyces. Isolates in the genera Rhodococcus, Streptosporangium, Luteipulveratus, and Nocardiopsis also showed inhibition. Twenty-five of the isolates with antifungal activity against P. destructans represent 15 novel Streptomyces spp. based on multilocus sequence analysis. Our results suggest that bats in western North America caves possess novel bacterial microbiota with the potential to inhibit P. destructans. IMPORTANCE This study reports the largest collection of actinobacteria from bats with activity against Pseudogymnoascus destructans, the fungal causative agent of white-nose syndrome. Using multigene analysis, we discovered 15 potential novel species. This research demonstrates that bats and caves may serve as a rich reservoir for novel Streptomyces species with antimicrobial bioactive compounds.KEYWORDS Actinobacteria, bats, caves, Pseudogymnoascus, Streptomyces, white-nose syndrome P resently, 90% of antibiotics are derived from microorganisms within the phylum Actinobacteria (1-3). The family Streptomycetaceae is particularly known for the production of chitinases capable of hydrolyzing the cell wall (4) and targeting ergosterol in the cell membrane of fungi (5). The rapid development of antibiotic resistance and the emergence of infectious diseases in humans and other animals, including bats and amphibians, have prompted the study of the bacterial microbiome and use for probiotic treatment in vertebrates (6, 7).

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“…1), sharing 99.5% sequence identity with the 16S rRNA genes of Streptomyces mexicanus and Streptomyces warraensis, their closest neighbours. Multi-locus sequence analysis (Rong and Huang 2012) based on the partial sequences of five housekeeping genes (atpD, gyrB, rpoB, recA and trpB) confirmed that strains C34, C38, C58 and C79 were not phylogenetically closely related to any Streptomyces type strains and formed a new centre of taxonomic variation in the genus Streptomyces, a result that was further underpinned by phenotypic and morphological tests . Thus the name S. leeuwenhoekii was proposed, with strain C34 (subsequently referred to as C34 T ) as the type strain and strains C38, C58 and C79 as additional members.…”

Section: Introductionmentioning

confidence: 90%

The ‘gifted’ actinomycete Streptomyces leeuwenhoekii

Castro

Razmilic

Gomez-Escribano

et al. 2018

Antonie van Leeuwenhoek

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Streptomyces leeuwenhoekii strains C34T , C38, C58 and C79 were isolated from a soil sample collected from the Chaxa Lagoon, located in the Salar de Atacama in northern Chile. These streptomycetes produce a variety of new specialised metabolites with antibiotic, anti-cancer and anti-inflammatory activities. Moreover, genome mining performed on two of these strains has revealed the presence of biosynthetic gene clusters with the potential to produce new specialised metabolites. This review focusses on this new clade of Streptomyces strains, summarises the literature and presents new information on strain C34T .

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Taxonomic evaluation of the Streptomyces hygroscopicus clade using multilocus sequence analysis and DNA–DNA hybridization, validating the MLSA scheme for systematics of the whole genus

Cited by 174 publications

References 39 publications

Population Genetic Analysis of Streptomyces albidoflavus Reveals Habitat Barriers to Homologous Recombination in the Diversification of Streptomycetes

Population Genetic Analysis of Streptomyces albidoflavus Reveals Habitat Barriers to Homologous Recombination in the Diversification of Streptomycetes

Western Bats as a Reservoir of Novel Streptomyces Species with Antifungal Activity

The ‘gifted’ actinomycete Streptomyces leeuwenhoekii

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