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Disease of Aquatic Organisms 96:113 Vol. 96: 113–123, 2011 DISEASES OF AQUATIC ORGANISMS Published September 9 doi: 10.3354/dao02389 Dis Aquat Org OPENPEN ACCESSCCESS Refined identification of Vibrio bacterial flora from Acanthasther planci based on biochemical profiling and analysis of housekeeping genes J. A. Rivera-Posada1,*, M. Pratchett1, A. Cano-Gomez2,3, J. D. Arango-Gomez4, L. Owens2,3 1ARC Centre of Excellence for Coral Reef Studies, James Cook University, Townsville, Queensland 4812, Australia 2School of Veterinary and Biomedical Sciences, James Cook University, Townsville Queensland 4812, Australia 3Australian Institute of Marine Science, Townsville, Queensland 4810, Australia 4School of Marine and Tropical Biology, James Cook University, Townsville, Queensland 4812, Australia ABSTRACT: We used a polyphasic approach for precise identification of bacterial flora (Vibrio - naceae) isolated from crown-of-thorns starfish (COTS) from Lizard Island (Great Barrier Reef, Australia) and Guam (USA, Western Pacific Ocean). Previous 16S rRNA gene phylogenetic analy- sis was useful to allocate and identify isolates within the Photobacterium, Splendidus and Harveyi clades but failed in the identification of Vibrio harveyi-like isolates. Species of the V. harveyi group have almost indistinguishable phenotypes and genotypes, and thus, identification by stan- dard biochemical tests and 16S rRNA gene analysis is commonly inaccurate. Biochemical profiling and sequence analysis of additional topA and mreB housekeeping genes were carried out for definitive identification of 19 bacterial isolates recovered from sick and wild COTS. For 8 isolates, biochemical profiles and topA and mreB gene sequence alignments with the closest relatives (GenBank) confirmed previous 16S rRNA-based identification: V. fortis and Photobacterium eurosenbergii species (from wild COTS), and V. natriegens (from diseased COTS). Further phylo- genetic analysis based on topA and mreB concatenated sequences served to identify the remain- ing 11 V. harveyi-like isolates: V. owensii and V. rotiferianus (from wild COTS), and V. owensii, V. rotiferianus, and V. harveyi (from diseased COTS). This study further confirms the reliability of topA−mreB gene sequence analysis for identification of these close species, and it reveals a wider distribution range of the potentially pathogenic V. harveyi group. KEY WORDS: Vibrio · Corallivores · Crown-of-thorns starfish · Harveyi clade · Splendidus clade Resale or republication not permitted without written consent of the publisher INTRODUCTION grate Vibrio spp. as part of their natural microflora, but also display susceptibility to this bacterium Vibrios constitute an important part of the bacterial (Gilles & Pearse 1986, Morgan 2000, Becker et al. microflora of numerous marine animals (Harris 1993, 2008). Moreover, remarkable similarities exist in the Oxley et al. 2002). Some species are also recognized clinical signs, time to death, histology, scanning as important pathogens of marine and estuarine ani- electron microscopy analysis, and identification of mals, causing substantial losses in commercial pro- vibrios as etiological agents (Morgan 2000, Becker et duction systems and natural waters throughout the al. 2004) with those described in experimentally- world (Kaysner & DePaola 2004). Particularly within induced diseased crown-of-thorns starfish (COTS; the Echinodermata, several species not only inte- Rivera-Posada et al. 2011). *Email: [email protected] © Inter-Research 2011 · www.int-res.com 114 Dis Aquat Org 96: 113–123, 2011 Resident bacteria constitute a critical barrier of omy studies, the Harveyi clade (Sawabe et al. 2007) resistance against colonization by exogenous mi- includes 10 Vibrio species: V. harveyi, V. campbellii, crobes, preventing tissue invasion by pathogens V. rotiferianus, V. alginolyticus, V. parahaemolyticus, (Guarner & Malagelada 2003). This function is ac - V. mytili, V. natriegens, the newly described species complished through different mechanisms, including V. azureus (Yoshizawa et al. 2009), V. owensii (Cano- (1) secretion of antibacterial substances to reduce the Gomez et al. 2010), and V. sagamiensis (Yoshizawa et number of viable pathogens, decrease bacterial al. 2010). Among this clade, the V. harveyi-related metabolism, or inhibit toxin production; (2) competi- species belonging to the so-called V. harveyi group tion for essential nutrients for pathogen survival; (V. harveyi, V. campbellii, V. rotiferianus, and V. (3) supplementation with vitamins and short-chain owensii) are phenotypically and genetically indistin- fatty acids to the host tissues; (4) competition with guishable, sharing almost identical biochemical pro- pathogens preventing their adhesion to the intestine; files and 16S rRNA gene sequences (Gomez-Gil et al. (5) enhancement of the production of defensive 2004, Cano-Gomez et al. 2010). Therefore, conven- molecules in the host; and (6) direct uptake or tional culture-based techniques, biochemical tests, decomposition of organic matter or toxic material and 16S rRNA gene analysis frequently lead to produced by pathogenic bacteria (Lievin et al. 2000, misidentification of V. harveyi-like isolates (Pedersen Guarner & Malagelada 2003, Macfarlane & Macfar- et al. 1998, Vandenberghe et al. 2003, Gomez-Gil et lane 2003). Disrupting the bacterial ecological bal- al. 2004). Previous analyses of 16S rRNA gene ance in healthy organisms allows overgrowth of sequences allocated some Vibrio strains isolated pathogenic bacteria, and establishes a suitable envi- from wild and sick COTS in Lizard Island (Great Bar- ronment for disease induction. Maladies and physio- rier Reef [GBR], Australia) and Guam (USA) within logical manifestations such as intestinal inflamma- the Harveyi clade, and some of these clustered tion, digestive ulcers, and multiple organ failure have within the V. harveyi group (Rivera-Posada et al. been associated with microflora imbalances (Lemaire 2011). However, due to the low resolution of 16S et al. 1997, Zhang & Chen 2010). rRNA, we were prompted to perform additional bio- It is therefore important to compare bacterial com- chemical tests and sequence analysis of 2 additional munities in echinoderms and other related marine housekeeping genes in order to precisely identify invertebrates in order to understand the role of bac- these isolates at the species level. terial balances in the health of these organisms. Ben- Multilocus sequence analysis (MLSA) is a recent soussan et al. (1984) analyzed bacterial isolates of approach that employs sequence analysis of several digestive tracts in the asteroid Solaster sp. and the housekeeping genes in bacteria and subsequent holothurian Pseudostichopus villosus in stable phylo genetic analysis of their concatenated se - physicochemical conditions (constant environment), quences to delineate species and infer genetic rela- and reported that the most common bacteria isolated tionships (Gevers et al. 2005). For the Harveyi clade, from these echinoderms were Vibrio-like Gram - this method has been described as an alternative to negative rods, which constituted half of the total bac- the expensive and labor-intensive DNA−DNA hy - terial load; and that a clear separation existed be- bridization (Gomez Gil et al. 2003, Cano-Gomez et al. tween enteric bacterial communities and sediment 2009), still considered the gold standard for bacterial microflora. Moreover, the authors suggested that species delineation (Stackebrandt et al. 2002). How- microflora of echinoderms, and in particular of the ever, MLSA is costly, time consuming, and requires a Asteroidea, has a more specialized tendency to the considerable amount of experience to analyze, con- catabolism of organic compounds; and they found a catenate, and construct phylogenies with DNA less diversified micro flora in echinoderms in compar- sequences of multiple loci. Recent efforts have ison with sediment microflora. focused on the design of a fast, practical, but still Species of the Harveyi clade have been described accurate identification method for Vibrio harveyi- as major pathogens to aquatic animals, causing dis- related species as an alternative to 16S rRNA gene ease outbreaks responsible for severe economic analysis and DNA−DNA hybridization. Short-term losses in the aquaculture industry worldwide. In- epidemiology studies or environmental surveys, for creasing infections in marine vertebrates and inver- example, involve a high number of isolates to be tebrates and even in humans have been linked to identified rapidly and efficiently. In these cases, and increased marine temperatures with diffusion of under the evidences pointing to the Harveyi clade, pathogens to higher latitudes (Bossart 2007, Igbinosa the number of genes sequenced could be minimized & Okoh 2008). According to current molecular taxon- for a more practical identification (Thompson et al. Rivera-Posada et al.: Identification of Vibrio in Acanthasther planci 115 2007, Cano-Gomez et al. 2011). While more than 5 obtained at Lizard Island (GBR): 5 isolated from wild genes should be analyzed for taxonomic studies of COTS and 6 sick COTS induced from thiosulfate- cryptic bacterial species, the use of at least 2 inde- citrate-bile-sucrose agar (TCBS) injection (see pendent housekeeping genes has been suggested Rivera-Posada et al. 2011). The other 8 strains were for bacterial identification purposes (Martens et al. obtained from COTS at Guam (USA, Mariana Archi- 2008). pelago): 3 from wild COTS and 5 from diseased A recent MLSA study
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