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View That Similar Evolutionary Paths of Host Adaptation Developed Independently in F Sjödin et al. BMC Genomics 2012, 13:268 http://www.biomedcentral.com/1471-2164/13/268 RESEARCH ARTICLE Open Access Genome characterisation of the genus Francisella reveals insight into similar evolutionary paths in pathogens of mammals and fish Andreas Sjödin1*, Kerstin Svensson1, Caroline Öhrman1, Jon Ahlinder1, Petter Lindgren1, Samuel Duodu2, Anders Johansson3, Duncan J Colquhoun2, Pär Larsson1 and Mats Forsman1 Abstract Background: Prior to this study, relatively few strains of Francisella had been genome-sequenced. Previously published Francisella genome sequences were largely restricted to the zoonotic agent F. tularensis. Only limited data were available for other members of the Francisella genus, including F. philomiragia, an opportunistic pathogen of humans, F. noatunensis, a serious pathogen of farmed fish, and other less well described endosymbiotic species. Results: We determined the phylogenetic relationships of all known Francisella species, including some for which the phylogenetic positions were previously uncertain. The genus Francisella could be divided into two main genetic clades: one included F. tularensis, F. novicida, F. hispaniensis and Wolbachia persica, and another included F. philomiragia and F. noatunensis. Some Francisella species were found to have significant recombination frequencies. However, the fish pathogen F. noatunensis subsp. noatunensis was an exception due to it exhibiting a highly clonal population structure similar to the human pathogen F. tularensis. Conclusions: The genus Francisella can be divided into two main genetic clades occupying both terrestrial and marine habitats. However, our analyses suggest that the ancestral Francisella species originated in a marine habitat. The observed genome to genome variation in gene content and IS elements of different species supports the view that similar evolutionary paths of host adaptation developed independently in F. tularensis (infecting mammals) and F. noatunensis subsp. noatunensis (infecting fish). Keywords: Francisella, Next-generation sequencing, Recombination, Fish, Genetics, Evolution Background The known diversity of the genus Francisella has re- Tularemia is a zoonotic disease caused by the highly in- cently expanded substantially and the boundaries be- fectious, virulent, Gram-negative bacterium Francisella tween taxonomic units within the genus is currently tularensis. Due to its infectious nature, ease of dissemin- under debate [2,3]. In mammals, including man, the dis- ation and associated high fatality rate (especially from ease tularemia is caused by two F. tularensis subspecies: respiratory infection), F. tularensis has been included in subsp. tularensis (type A, endemic in North America) military biological weapons programs and is regarded as and subsp. holarctica (type B, found throughout the one of the top six agents which have a high potential for Northern hemisphere) [4]. Nearly all fatalities due to tu- misuse in bioterrorism [1]. laremia are caused by F. tularensis type A infections, for which mortality rates up to 30% have been reported [5]. In contrast, F. tularensis type B causes a milder disease, for which fatalities rarely occur. A third accepted sub- * Correspondence: [email protected] species, F. tularensis subsp. mediasiatica is found in 1Division of CBRN Security and Defence, FOI - Swedish Defence Research Agency, Umeå, Sweden central Asia. This subspecies has been found to display Full list of author information is available at the end of the article level of virulence comparable to strains of subspecies © 2012 Sjödin 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. Sjödin et al. BMC Genomics 2012, 13:268 Page 2 of 13 http://www.biomedcentral.com/1471-2164/13/268 holarctica and very rarely cause human infections [6,7]. day strains can be divided into two main genetic clades Disease in humans has also been presented following op- occupying continental and aquatic habitats and provide portunistic infection by F. novicida (in individuals with a evidence that similar evolutionary paths of host adapta- weakened immune system) and F. philomiragia (in indi- tions have occurred independently in F. tularensis (in- viduals with a weakened immune system exposed to sea fecting mammals) and F. noatunensis subsp. noatunensis water) [8-10]. (infecting fish). AnumberofFrancisella lineages also exist that do not appear to be associated with human disease. Strains Results closely related to F. philomiragia, which have recently Bacterial strains and classifications been designated as Francisella noatunensis, have been Here, we present 24 novel genome sequences represent- identified as etiological agents of Francisellosis in fish ing all major subclades of the Francisella genus (Table 1), [11-15]. F. noatunensis is further divided into two sub- with the exception of the recently discovered F. cantonensis species, subsp. noatunensis [16] and subsp. orientalis [27]. The data doubles the number of published Francisella [17,18]. Recent published studies have also identified genomes and significantly extends the known range of several new related and as yet uncultured forms of genetic diversity. The studied material includes seven pre- Francisella from soil and water [19-23], as well as tick viously unsequenced F. noatunensis isolates and a single endosymbionts with high similarity to F. tularensis representative from the tick endosymbiont group [31]. (Francisella-like endosymbionts) [24]. One isolated tick In addition, representatives of Fa. hongkongensis [29] endosymbiont has inaccurately been designated Wolbachia and P. salmonis [32], both of which are related to the persica [25], incorrectly placing it within the alpha- genus Francisella, were also sequenced. Interestingly, proteobacteria [26]. Further, a marine ciliate endosymbiont Francisella strain 3523 [33,34] appeared to belong to the has been proposed to represent ‘Candidatus F. noatunensis F. hispaniensis clade and not the F. novicida clade as subsp. endociliophora’ [23] and a bacterium isolated from reported previously [34]. an air-conditioning system has been tentatively classified Overall, a major bifurcation into two genetic lineages was as Francisella cantonensis [27]. Thus, in recent years the identified (Figure 1) with clade 1 comprising F. tularensis, existence of substantial sub-species diversity within the F. novicida, F. hispaniensis and W. persica, and clade 2 Francisella genus has become increasingly apparent. Mem- containing F. noatunensis and F. philomiragia. bers of Francisella appear to be associated with a multi- tude of different ecological niches, ranging from specialised Francisella whole-genome phylogeny and endosymbionts and pathogens with different host spec- average nucleotide identities trums, to generalists believed capable of a free-living Whole-genome alignments were produced using pro- existence. gressiveMauve [35]. A phylogeny based on core genome There are several reasons for sequencing Francisella single nucleotide polymorphisms is shown in Figure 1. strains other than those belonging to F. tularensis. Ana- Analysis of the whole-genome phylogeny showed that lysis of gene content and genetic relationships may help strains of F. philomiragia and F. noatunensis subsp. to improve our understanding of the biology and evolution noatunensis formed sister clades, while strains of of these bacteria, including that of the human pathogen F. noatunensis subsp. orientalis divergedatamorebasal F. tularensis. Sequencing multiple strains of environmen- position, indicating the newly named species F. noatunensis tal Francisella may also reveal important sequence differ- is paraphyletic. This interpretation was supported by ences between environmental species and F. tularensis. an analysis of average nucleotide identities (ANI): ANI This would allow the design of increasingly specific for F. philomiragia compared to F. noatunensis subsp. F. tularensis detection assays for use in anti-bioterrorism noatunensis is higher (95%) than F. philomiragia com- applications and epidemiological studies, particularly im- pared to F. noatunensis subsp. orientalis (92–93%) portant since current methods frequently falsely detect Additional file 1. F. tularensis in environmental samples [28]. Phylogenetic inference using whole-genome data and The genome sequence data generated by the present 16 S ribosomal RNA genes resulted in incongruent top- study represents a considerable advancement of know- ologies. The phylogenetic position of F. philomiragia ledge of the genus Francisella and includes genome (Figure 1) was different from previous publications of sequences for 18 environmental Francisella strains, four phylogenies calculated based on 16 S ribosomal RNA F. tularensis and two distant but genetically related species genes (Additional file 2) [13,14]. Fangia hongkongensis [29] and Piscirickettsia salmonis [30]. Here we describe the population structure of the Analysis of Francisella pan and core genomes genus Francisella, suggest that ancestral Francisella Based on the analysed gene orthologs, the core genome strains originated in marine habitats, show that present- of the genus Francisella contained 803 genes (Figure 2A). Sjödin et al. BMC Genomics 2012, 13:268 Page 3 of 13 http://www.biomedcentral.com/1471-2164/13/268
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