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Comparative Genomics of the Aeromonadaceae Core Oligosaccharide Biosynthetic Regions

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Comparative Genomics of the Aeromonadaceae Core Oligosaccharide Biosynthetic Regions International Journal of Molecular Sciences Article Comparative Genomics of the Aeromonadaceae Core Oligosaccharide Biosynthetic Regions Gabriel Forn-Cuní, Susana Merino and Juan M. Tomás * Department of Genética, Microbiología y Estadística, Universidad de Barcelona, Diagonal 643, 08071 Barcelona, Spain; [email protected] (G.-F.C.); [email protected] (S.M.) * Correspondence: [email protected]; Tel.: +34-93-4021486 Academic Editor: William Chi-shing Cho Received: 7 February 2017; Accepted: 26 February 2017; Published: 28 February 2017 Abstract: Lipopolysaccharides (LPSs) are an integral part of the Gram-negative outer membrane, playing important organizational and structural roles and taking part in the bacterial infection process. In Aeromonas hydrophila, piscicola, and salmonicida, three different genomic regions taking part in the LPS core oligosaccharide (Core-OS) assembly have been identified, although the characterization of these clusters in most aeromonad species is still lacking. Here, we analyse the conservation of these LPS biosynthesis gene clusters in the all the 170 currently public Aeromonas genomes, including 30 different species, and characterise the structure of a putative common inner Core-OS in the Aeromonadaceae family. We describe three new genomic organizations for the inner Core-OS genomic regions, which were more evolutionary conserved than the outer Core-OS regions, which presented remarkable variability. We report how the degree of conservation of the genes from the inner and outer Core-OS may be indicative of the taxonomic relationship between Aeromonas species. Keywords: Aeromonas; genomics; inner core oligosaccharide; outer core oligosaccharide; lipopolysaccharide 1. Introduction Aeromonads are an heterogeneous group of Gram-negative bacteria emerging as important pathogens of both gastrointestinal and extraintestinal diseases in a great evolutionary range of animals: from fish to mammals, including humans [1]. In recent years, as our knowledge about Aeromonas taxonomy, biology and pathogenicity has increased, and the number of reported infections caused by these microorganisms in healthy and immunocompromised patients has also spiked [2]. Despite the fact that, in humans, the most common complications derived from these pathogens are mild and easily tractable, they can present a serious risk in immunocompromised patients, causing severe septicaemia and even death [3]. Therefore, increasing our knowledge on the virulence factors governing aeromonad pathogenicity is of crucial importance to prevent the increasing complications caused by these bacteria. The virulence and pathogenicity of Aeromonas is multifactorial, varies between species and strains, and has been linked to, among others, toxins, flagella, secretion systems, outer-membrane proteins and capsules, and surface polysaccharides, such as lipopolysaccharides (LPSs) [4]. LPSs, also known as endotoxins, are an integral part of the outer membrane for the great majority of Gram-negative bacteria, covering approximately the 75% of its surface and playing a crucial role on its organization and structure [5]. Although the exposed sections of LPSs are highly variable between species—and sometimes even between strains—LPSs molecules follow the same structural architecture depicted in Figure1: a hydrophobic lipid component, the lipid A, bound to a hydrophilic polysaccharide [ 5]. The polysaccharide is composed by the core oligosaccharide (Core-OS), and the more variable O-specific chain (O-antigen), which may be present (Smooth LPS) or not (Rough LPS). The Core-OS can be further subdivided into the inner core and outer core. On the one side, the inner core, containing Int. J. Mol. Sci. 2017, 18, 519; doi:10.3390/ijms18030519 www.mdpi.com/journal/ijms Int. J. Mol. Sci. 2017, 18, 519 2 of 12 moreInt. J. Mol.variable Sci. 2017 O-specific, 18, 519 chain (O-antigen), which may be present (Smooth LPS) or not (Rough LPS).2 of 12 The Core-OS can be further subdivided into the inner core and outer core. On the one side, the inner core,a high containing proportion a ofhigh unusual proportion sugars, of predominantlyunusual sugars, one predominantly to three 3-deoxy- oneD to-manno-oct-2-ulosonic three 3-deoxy-D-manno- acid oct-2-ulosonic(Kdo) residues acid and two(Kdo) or residues three heptoses and two (Hep), or th tendsree heptoses to be evolutionarily (Hep), tends conserved to be evolutionarily within and a conservedtaxonomic within family orand genus, a taxonomic and is the family part boundor genus, to theand lipid is the A [part6]. On bound the other to the side, lipid the A outer [6]. On core the is otherusually side, formed the outer by common core is sugars—as usually formed hexoses by and common hexosamines—present sugars—as hexoses more and variability, hexosamines— and this presentis the region more boundvariability, to the and O-antigen, this is the if presentregion bound [6]. to the O-antigen, if present [6]. FigureFigure 1. StructureStructure andand genomic genomic organization organization of theof theAeromonas Aeromonas piscicola piscicolaAH-3 AH-3 lipopolysaccharide lipopolysaccharide (LPS). (LPS).(a) Chemical (a) Chemical structure structure of the ofA. thepiscicola A. piscicolaAH-3 LPS.AH-3 From LPS. clearerFrom clearer to darker, to darker, the carbohydrates the carbohydrates of the ofinner the coreinner oligosaccharide, core oligosaccharid outer coree, outer oligosaccharide, core oligosaccharide, and O-antigen and (only O-antigen the first (only two molecules)the first two are molecules)shown. The are name shown. of the The proteins name catalysing of the proteins each reaction catalysing is shown each in reaction each link is betweenshown in components; each link betweenand (b) Genomic components; organization and (b) ofGenomic the A. piscicola organizationAH-3 genesof thecoding A. piscicola for the AH-3 proteins genes taking coding part for in the the proteinsLPS biosynthesis. taking part in the LPS biosynthesis. WhileWhile the the AeromonasAeromonas LPSLPS follows follows the the same same architectural architectural pattern pattern as as the the rest of Gram-negative bacteria,bacteria, this this molecule molecule displays displays remarkable remarkable diversity diversity across across species species of of this genus. We We previously previously reportedreported the the molecular molecular structure structure of ofthe the LPS LPS from from wild-type wild-type A. hydrophilaA. hydrophila AH-1AH-1 [7], A. [ 7piscicola], A. piscicola AH-3 (formerlyAH-3 (formerly A. hydrophilaA. hydrophila AH-3) [8] AH-3)and A. [salmonicida8] and A. subspsalmonicida. salmonicida subsp [9].. salmonicidaFurthermore,[9 we]. Furthermore,characterized thewe genes characterized coding for the the genes proteins coding taking for part the proteinsin the assembly taking partof both in thethe inner assembly and outer of both LPS the core inner of theseand outer species, LPS which coreof are these located species, in three which different are located genomic in three regions: different the genomicwa Regions regions: 1 to 3 the [8,9].wa Roughly,Regions 1 wa to 3Region [8,9]. Roughly,1 containswa genesRegion relate 1 containsd to the genes outer related core, whereas to the outer wa Regions core, whereas 2 andwa 3 codeRegions for enzymes2 and 3 code related for enzymesto the inner related core biosynthesis to the inner core (Figur biosynthesise 1). To date, (Figure the conservation1). To date, theand conservation characterization and ofcharacterization these LPS biosynthetic of these LPS regions, biosynthetic which may regions, be a whichkey factor may governing be a key factor pathogenicity, governing remains pathogenicity, to be studiedremains in to the be studiedrest of Aeromonadaceae in the rest of Aeromonadaceae. In this article,. we In thisanalyse article, the wesynteny analyse of the three synteny Core-OS of the biosynthesisthree Core-OS gene biosynthesis clusters across gene all clusters the publicly across allavailable the publicly Aeromonas available genomesAeromonas and predict,genomes for andthe firstpredict, time, for a theconserved first time, inner a conserved LPS oligosaccharide inner LPS oligosaccharide core substructure core substructurein all the species in all of the Aeromonas species of genus.Aeromonas genus. 2.2. Results Results AA total total of of 170 170 genomes comprising a variable number ofof strainsstrains andand biovarsbiovars fromfromthe theAeromonas Aeromonas speciesspecies AA.. allosaccharophila allosaccharophila,, AA.. aquatica aquatica,, AA.. australiensis australiensis,, AA.. bestiarum bestiarum,, AA.. bivalvium bivalvium,, AA.. caviae caviae,, AA.. dhakensis dhakensis, , AA.. diversa diversa,, AA.. encheleia encheleia, ,AA.. enteropelogenes enteropelogenes, A, .A. eucreophila eucreophila, A,. A.finlandiensis finlandiensis, A,. A.fluvialis fluvialis, A., hydrophilaA. hydrophila, A. , jandaeiA. jandaei, A., A.lacus lacus, A,. A.media media, A,. A.molluscorum molluscorum, A,.A. piscicola piscicola, A, .A. popoffii popoffii, A, A.. rivuli rivuli, A, A.. salmonicida salmonicida, ,AA.. sanarellii sanarellii, , A. schubertii, A. simiae, A. sobria, A. taiwanensis, A. tecta, A. veronii, and other uncharacterized strains Int.Int. J. J. Mol. Mol. Sci. Sci. 20172017, ,1818, ,519 519 33 of of 12 12 A. schubertii, A. simiae, A. sobria, A. taiwanensis, A. tecta, A. veronii, and other uncharacterized strains (Aeromonas sp.) were retrieved from the National Center for Biotechnology Information genome (Aeromonas sp.) were retrieved from the National Center
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