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10 the Family Colwelliaceae John P 10 The Family Colwelliaceae John P. Bowman Food Safety Centre, Tasmanian Institute of Agriculture, University of Tasmania, Hobart, TAS, Australia Taxonomy, Historical, and Current Short Description Taxonomy, Historical, and Current Short of the Family Colwelliaceae Ivanova Description of the Family Colwelliaceae VP et al. 2004, 1773VP .........................................179 Ivanova et al. 2004, 1773 Molecular Analyses . ..................................180 Col.well.i0a.ce.ae. N.L. fem. n. Colwellia, type genus of the fam- ily; suff. -aceae, ending to denote a family; N.L. fem. pl. n. Phenotypic Properties . ..................................181 Colwelliaceae, the Colwellia family. The family Colwelliaceae was first described by Ivanova and Genus Colwellia Deming et al. 1988, 328AL ...............181 colleagues (2004) as part of an effort to create taxonomic har- mony within a large clade of almost exclusively marine bacteria Genus Thalassomonas Macia´n et al. 2001, 1283 . 187 located within class Gammaproteobacteria. This clade now rep- resents the order Alteromonadales (Bowman and McMeekin Enrichment, Isolation, and Maintenance Procedures . 187 2005) and consists of at least 22 genera as of late 2012. In addition to the genera Colwellia and Thalassomonas, Genome-Based and Genetic Studies . .....................191 the other members of the order include Aesturaiibacter, Agarivorans, Algicola, Aliagarivorans, Alkalimonas, Ecology . ...............................................192 Alishewanella, Alteromonas, Bowmanella, Catenovulum, Ferri- monas, Glaciecola, Idiomarina, Moritella, Oceanisphaera, Para- Applications ...............................................193 ferrimonas, Pseudoalteromonas, Psychromonas, Rheinheimera, Salinimonas, and Shewanella. The order Alteromonadales is subdivided into several families; besides Colwelliaceae these Abstract families include Alteromonadaceae, Ferrimonadaceae, Idio- The family Colwelliaceae is part of the order Alteromonadales marinaceae, Moritellaceae, Pseudoalteromonadaceae, and within the class Gammaproteobacteria and currently comprises Shewanellaceae. The description of new genera since 2004 the type genus Colwellia and the genus Thalassomonas. prompts description of new families or perhaps more usefully, Collectively, Colwelliaceae encompasses at least 19 species. Both when more genome data becomes available, a taxonomic genera are strictly marine in terms of distribution and appear as reappraisal of the entire order. curved to straight rod-shaped cells that form primarily The genus Colwellia was first described by Deming et al. nonpigmented colonies, possess a polar or subpolar flagellum, (1988) on the basis of 5S rRNA sequence data of two very and are catalase and oxidase positive. Metabolism varies between psychrophilic strains including strain ATCC 27364T the two genera, with Colwellia species being facultatively anaer- (NRC1004) isolated from Flounder eggs collected near Trond- obic and able to grow fermentatively and also by using at least heim, Norway, and barophilic strain BNL-1T, collected from nitrate as an electron acceptor. Most Thalassomonas species are surface sediment of the Puerto Rico Trench at a depth of instead strictly aerobic; however further study is required to 7,410 m. Strain ATCC 27364T, which possessed an unusual confirm this. Both members of Colwelliaceae have attracted bright red prodigiosin-like pigment (D’’Aoust and Gerber interest in terms of extremophilic environmental research and 1974) and produced a self-toxic growth response, was initially biotechnological investigations. The genus Colwellia contains named by Da´oust and Kushner (1972)‘‘Vibrio psychroerythrus.’’ several obligately psychrophilic (cold-requiring) and piezophilic ATCC 27364T and BNL-1T were designated Colwellia (pressure-requiring) species that synthesize omega-3 polyunsat- psychrerythraea, the type species, and Colwellia hadaliensis, urated fatty acids while a number of Thalassomonas species respectively, by Deming and colleagues (1988). Subsequently possess potent agarolytic activity. The species Colwellia a further 10 species have since been added to the genus, deriving psychrerythraea represents a model for understanding how bac- from a diversity of marine environments, and include teria thrive at freezing temperatures. C. demingiae, C. hornerae, C. psychrotropica, C. rossensis E. Rosenberg et al. (eds.), The Prokaryotes – Gammaproteobacteria, DOI 10.1007/978-3-642-38922-1_230, # Springer-Verlag Berlin Heidelberg 2014 180 10 The Family Colwelliaceae . Fig. 10.1 16S rRNA gene sequence-based neighbor-joining tree (distances based on maximum likelihood algorithm) showing the position of members of the family Colwelliaceae (which are shown in colored type) within the order Alteromonadales. Thermotoga maritima and Coprothermobacter platensis represented out-groups. Sequences used come from the type strains of the following species (GenBank accession code): Colwellia piezophila (NR_024805), Colwellia maris (NR_024635), Colwellia rossensis (NR_025957), Colwellia psychrotropica (NR_026055), Colwellia psychrerythraea (NR_037047), Colwellia aestuarii (NR_043509), Colwellia asteriadis (EU599214), Colwellia chukchiensis (FJ889599), Colwellia hornerae (JN175346), Colwellia demingiae (U85845), Colwellia polaris (DQ007434), Thalassomonas viridans (NR_042048), Thalassomonas haliotis (NR_041662), Thalassomonas actiniarum (NR_041661), Thalassomonas agariperforans (HM237288), Thalassomonas ganghwensis (NR_025717), Thalassomonas agarivorans (NR_043649), Thalassomonas loyana (NR_043066), Agarivorans albus (NR_024788), Agarivorans gilvus (GQ200591), Aliagarivorans marinus (FJ167390), Aliagarivorans taiwanensis (FJ167391), Algicola sagamiensis (NR_027234), Alishewanella fetalis (AF144407), Alkalimonas amylolytica (AF250323), Alteromonas macleodii (Y18228), Bowmanella denitrificans (DQ343294), Catenovulum agarivorans (GQ262000), Ferrimonas balearica (CP002209), Glaciecola punicea (U85853), Idiomarina abyssalis (NR_024891), Moritella marina (AB038033), Oceanisphaera litoralis (AJ550470), Paraferrimonas sedimenticola (NR_041444), Pseudoalteromonas haloplanktis (X67024), Psychromonas antarctica (Y14697), Rheinheimera baltica (AJ441080), Salinimonas chungwhensis (AY553295), Shewanella putrefaciens (X81623) (Bowman et al. 1998), C. maris (Yumoto et al. 1998), (Thompson et al. 2006), T. actiniarum, T. haliotis (Hosoya C. piezophila (Nogi et al. 2004), C. aestuarii (Jung et al. 2006), et al. 2009), and T. agariperforans (Park et al. 2011). C. polaris (Zhang et al. 2008), C. asteriadis (Choi et al. 2010), and C. chukchiensis (Yu et al. 2011). Thalassomonas the sister genus of Colwellia includes seven Molecular Analyses species as of late 2012. The type species, Thalassomonas viridans, was isolated from a Mediterranean sea oyster (Macia´n et al. Colwellia and Thalassomonas species cluster together and pos- 2001) and subsequent additional species also derive from sess a maximum 16S rRNA gene sequence dissimilarity of a diverse range of strictly marine sites mainly located in temper- approximately 7 %. Thalassomonas species in most 16S rRNA ate to tropical regions. These species include T. ganghwensis gene-based trees are not monophyletic but form two (Yi et al. 2004), T. agarivorans (Jean et al. 2006), T. loyana paraphyletic sub-lineages (> Fig. 10.1). One sub-lineage The Family Colwelliaceae 10 181 contains the species T. viridans, T. actiniarum, and T. haliotis evolved (Franzmann 1996). Whether the predilection towards while the second contains T. ganghwensis, T. loyana, psychrophily in the genus Colwellia reflects a bias of isolation T. agarivorans, and T. agariperforans. Colwellia is on the other from cold marine sites is unknown; however it is reasonable hand clearly monophyletic with C. chukchiensis, C. polaris, and to assume at least at this stage that Colwellia is by and large C. aestuarii forming a peripheral relatively distinct sub-lineage. a highly cold-adapted lineage of bacteria, a rather rare feature The next closest related genera to family Colwelliaceae amongst cultivated bacteria and archaea. The geographical dis- include Agarivorans (Kurahashi and Yokota 2004) and tribution of Colwellia is broad but appears to be strictly marine Aliagarivorans (Jean et al. 2009), which currently are not affili- (see > Ecology section). ated with a family level taxon. Available data however does not In comparison to the genus Thalassomonas, Colwellia species lend convincing justification that either of these genera should have lower temperature growth ranges and optima for growth be placed in Colwelliaceae, either on the basis of 16S rRNA gene- and in general are slightly larger (range 1–5 Â 0.4–1.0 mm) based phylogeny or on the basis of phenotypic data. Further data and are pronouncedly more curved in shape. Colwellia is is required and as mentioned previously a more in-depth also facultatively anaerobic and able to grow either by aerobic genome sequence data-based appraisal is required to further oxidation, fermentation of carbohydrates, and by anaerobic develop the higher level taxonomy amongst the members of respiration with nitrate and other electron acceptors such as order Alteromonadales. manganese (see > Ecology section) but likely unable to use ferric iron as electron acceptor. Acetate and a variety of other simple compounds can serve as electron donors. Most species Phenotypic Properties can form chitinases but so far none have been found that degrade agar. The species generally grow on a range
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