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A Phylogenetic Approach in Actinobacteria

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A Phylogenetic Approach in Actinobacteria On the nature of fur evolution: A phylogenetic approach in Actinobacteria Catarina L Santos, João Vieira, Fernando Tavares, David R Benson, Louis S Tisa, Alison M Berry, Pedro Moradas-Ferreira, Philippe Normand To cite this version: Catarina L Santos, João Vieira, Fernando Tavares, David R Benson, Louis S Tisa, et al.. On the nature of fur evolution: A phylogenetic approach in Actinobacteria. BMC Evolutionary Biology, BioMed Central, 2008, 8 (185), pp.1-14. 10.1186/1471-2148-8-185. halsde-00354531 HAL Id: halsde-00354531 https://hal.archives-ouvertes.fr/halsde-00354531 Submitted on 30 May 2020 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. BMC Evolutionary Biology BioMed Central Research article Open Access On the nature of fur evolution: A phylogenetic approach in Actinobacteria Catarina L Santos*1,2, João Vieira1, Fernando Tavares1,2, David R Benson3, Louis S Tisa4, Alison M Berry5, Pedro Moradas-Ferreira1,6 and Philippe Normand7 Address: 1IBMC – Instituto de Biologia Molecular e Celular, Universidade do Porto, Rua do Campo Alegre, 823, 4150-180 Porto, Portugal, 2Faculdade de Ciências da Universidade do Porto, Departamento de Botânica, Rua do Campo Alegre 1191, 4150-181 Porto, Portugal, 3Department of Molecular and Cell Biology, University of Connecticut, Storrs, CT 06279, USA, 4Department of Microbiology, University of New Hampshire, Durham, NH, 03824, USA, 5Department of Plant Sciences, Mail Stop 1, PES Building, University of California, Davis, CA 95616, USA, 6Instituto de Ciências Biomédicas Abel Salazar, Lg. Prof. Abel Salazar, 4099-003 Porto, Portugal and 7UMR 5557 CNRS Ecologie Microbienne, IFR41 Bio- Environnement et Santé, Université Lyon 1, 43 Bd du 11 novembre 1918, 69622 Villeurbanne Cedex, France Email: Catarina L Santos* - [email protected]; João Vieira - [email protected]; Fernando Tavares - [email protected]; David R Benson - [email protected]; Louis S Tisa - [email protected]; Alison M Berry - [email protected]; Pedro Moradas- Ferreira - [email protected]; Philippe Normand - [email protected] * Corresponding author Published: 25 June 2008 Received: 31 December 2007 Accepted: 25 June 2008 BMC Evolutionary Biology 2008, 8:185 doi:10.1186/1471-2148-8-185 This article is available from: http://www.biomedcentral.com/1471-2148/8/185 © 2008 Santos et al; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Abstract Background: An understanding of the evolution of global transcription regulators is essential for comprehending the complex networks of cellular metabolism that have developed among related organisms. The fur gene encodes one of those regulators – the ferric uptake regulator Fur – widely distributed among bacteria and known to regulate different genes committed to varied metabolic pathways. On the other hand, members of the Actinobacteria comprise an ecologically diverse group of bacteria able to inhabit various natural environments, and for which relatively little is currently understood concerning transcriptional regulation. Results: BLAST analyses revealed the presence of more than one fur homologue in most members of the Actinobacteria whose genomes have been fully sequenced. We propose a model to explain the evolutionary history of fur within this well-known bacterial phylum: the postulated scenario includes one duplication event from a primitive regulator, which probably had a broad range of co- factors and DNA-binding sites. This duplication predated the appearance of the last common ancestor of the Actinobacteria, while six other duplications occurred later within specific groups of organisms, particularly in two genera: Frankia and Streptomyces. The resulting paralogues maintained main biochemical properties, but became specialised for regulating specific functions, coordinating different metal ions and binding to unique DNA sequences. The presence of syntenic regions surrounding the different fur orthologues supports the proposed model, as do the evolutionary distances and topology of phylogenetic trees built using both Neighbor-Joining and Maximum-Likelihood methods. Conclusion: The proposed fur evolutionary model, which includes one general duplication and two in-genus duplications followed by divergence and specialization, explains the presence and diversity of fur genes within the Actinobacteria. Although a few rare horizontal gene transfer events Page 1 of 14 (page number not for citation purposes) BMC Evolutionary Biology 2008, 8:185 http://www.biomedcentral.com/1471-2148/8/185 have been reported, the model is consistent with the view of gene duplication as a main force of microbial genomes evolution. The parallel study of Fur phylogeny across diverse organisms offers a solid base to guide functional studies and allows the comparison between response mechanisms in relation with the surrounding environment. The survey of regulators among related genomes provides a relevant tool for understanding the evolution of one of the first lines of cellular adaptability, control of DNA transcription. Background Among the Fur-like proteins, those responding to oxida- Fur proteins form a ubiquitous family of metal-responsive tive stress by regulating a downstream catalase-peroxidase transcription factors known to regulate the transcription have been the most studied in the Actinobacteria [19,21- of several different genes in many diverse bacterial line- 24]. However, despite detailed knowledge on catalase- ages. Upon binding to a metal ion, a conformational peroxidase regulation and the variety of functional and change is induced in the Fur regulator that promotes inter- structural studies on numerous microorganisms, very lit- action with a cognate DNA sequence, typically known as tle is known about the origin and molecular evolution of a Fur or iron box [1]. Initially, Fe (II) was thought to be the fur. The increasingly recognised importance of Fur as a vir- only metal able to play this role. In fact, Fur was initially ulence factor [24-26] and as a potential target for novel characterised as being an iron-responsive regulator of fer- antibiotics [10,25] would be better addressed with a ric iron uptake systems in Escherichia coli [2,3], hence its deeper knowledge on its evolutionary history. The enor- name. However, several studies have shown that Fur can mous diversity of Fur in terms of both required co-factors bind other metals – besides iron – as co-factors, and thus and regulated genes has led to several efforts to organise the range of known regulated genes became broader than the family [9,27]. what was initially thought. Fur will bind Fe (II) and regu- late iron homeostasis in several organisms [2,4-8]. How- The phylum Actinobacteria is comprised of Gram-positive ever, in addition to iron, different Fur homologues bacteria with an overall high Mol% G+C content. The pri- specifically require other divalent metals, including Zn2+, mary habitat for many of these bacteria is the soil, where Ni2+, Mn2+ or Co2+, in order to bind to their cognate pro- they degrade organic compounds and play an important moter targets [9-11]. These transition metal ions are con- role in mineralisation. The lineage also contains impor- sidered fundamental for bacterial growth, given that they tant secondary metabolite-producers and several impor- perform various essential functions in cellular metabo- tant pathogens and symbionts. The latter groups include lism. However, most of them are toxic at elevated levels. the mycobacterial agents of tuberculosis and leprosy and Therefore, a strict balance between their uptake and efflux, the nitrogen-fixing plant microsymbionts Frankia spp., effected by metalloregulators like Fur, is essential for among other ecologically and economically important homeostasis [12-15]. Excess amounts of these metal ions microorganisms [28]. Actinobacteria also inhabit aquatic elicit a number of stress conditions inside the cells, partic- systems, while others are associated with extreme environ- ularly oxidative stress [16]. Accordingly, some Fur-like ments such as acidic thermal springs [29], Antarctic rego- proteins, through sensing the availability of their specific lith [30] or gamma [31] and UV irradiated biotopes [32]. metal co-factor, are sensitive to the redox status of the cell, The ability to inhabit these different environments proba- establishing a relationship between these regulators and bly selects for the capacity to sense and cope with a wide the oxidative stress response [17-20]. range of metals, for which regulators of the Fur family are important. It is this diversity of habitats and lifestyles that Recent publications support a major role for Fur in the makes Actinobacteria such an excellent subject for an evo- regulation of various environmental conditions including lutionary study of a global regulator like
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