Abstract
Bacterial strains CNX-216T and CNU-914T were isolated from marine sediment samples collected from Palmyra Atoll and off Catalina Island, respectively. Both strains were Gram-negative and aerobic and produce deep-orange to pink colonies and alkaloid secondary metabolites. Cells of strain CNX-216T were short, non-motile rods, whereas cells of strain CNU-914T were short, curved rods with gliding motility. The DNA G+C contents of CNX-216T and CNU-914T were respectively 57.7 and 44.4 mol%. Strains CNX-216T and CNU-914T contained MK-7 as the predominant menaquinone and iso-C15 : 0 and C16 : 1ω5c as the major fatty acids. Phylogenetic analyses revealed that both strains belong to the order Cytophagales in the phylum Bacteroidetes. Strain CNX-216T exhibited low 16S rRNA gene sequence identity (87.1 %) to the nearest type strain, Cesiribacter roseus 311T, and formed a well-supported lineage that is outside all currently described families in the order Cytophagales. Strain CNU-914T shared 97.6 % 16S rRNA gene sequence identity with ‘Porifericola rhodea’ N5EA6-3A2B and, together with ‘Tunicatimonas pelagia’ N5DB8-4 and four uncharacterized marine bacteria isolated as part of this study, formed a lineage that is clearly distinguished from other families in the order Cytophagales. Based on our polyphasic taxonomic characterization, we propose that strains CNX-216T and CNU-914T represent novel genera and species, for which we propose the names Mooreia alkaloidigena gen. nov., sp. nov. (type strain CNX-216T = DSM 25187T = KCCM 90102T) and Catalinimonas alkaloidigena gen. nov., sp. nov. (type strain CNU-914T = DSM 25186T = KCCM 90101T) within the new families Mooreiaceae fam. nov. and Catalimonadaceae fam. nov.
Marine environments harbour remarkable levels of bacterial diversity (Giovannoni et al., 1990), much of which appears to be uniquely marine. The vast majority of this diversity has yet to be cultured (Rappé & Giovannoni, 2003), creating a major void between that which is known to exist and that which has been subjected to systematic evaluation. Among the bacteria frequently observed in marine samples are members of the phylum Bacteroidetes (formerly the Cytophaga–Flavobacteria–Bacteroidetes group). Members of this phylum are known to colonize marine particles (Gómez-Pereira et al., 2012) and have been reported to play a major role in the degradation of organic matter in marine ecosystems (Kirchman, 2002). While the phylum Bacteroidetes has been the subject of considerable taxonomic revision (Gupta, 2004), it is currently comprised of four large classes (Bacteroidia, Cytophagia, Flavobacteria and Sphingobacteriia) and corresponding orders (Bacteroidales, Cytophagales, Flavobacteriales and Sphingobacteriales) (Ludwig et al., 2010).
Within the phylum Bacteroidetes, the order Cytophagales includes a morphologically diverse assemblage of unicellular Gram-negative bacteria, many of which display gliding motility (Reichenbach, 2006). Defining characteristics of the order Cytophagales include the production of flexirubin-type pigments, starch hydrolysis and the possession of menaquinone 7 (MK-7) (Reichenbach, 2006). As with other members of the phylum Bacteroidetes, many of the species in the order Cytophagales occur in marine or saline environments. At the time of writing, there are four recognized families within this order (Cyclobacteriaceae, Cytophagaceae, Flammeovirgaceae and Rhodothermaceae) and 58 genera (http://www.bacterio.cict.fr/classifphyla.html).
We cultured two alkaloid-producing strains of Gram-negative bacteria from marine sediment samples collected from the remote Pacific island atoll of Palmyra (strain CNX-216T) and off the Channel Islands, California (strain CNU-914T). Based on a polyphasic taxonomic analysis, we propose that these two strains represent two novel genera and species within the proposed families Mooreiaceae fam. nov. and Catalimonadaceae fam. nov. within the order Cytophagales.
Marine sediment samples were collected in sterile Whirl-pac bags by divers and dried overnight in a laminar flow hood. Dried sediments were stamped onto P1 agar plates (18.0 g agar, 1 l filtered seawater) using sterile foam plugs as described previously (Jensen et al., 2005) and incubated at room temperature (approx. 25 °C) for 2 months. The amount of sediment added to each plate varied depending on how well it adhered to the foam plug, but was estimated in most cases to be <100 mg. Both strains were subsequently obtained in pure culture by repeated streaking onto medium A1 (10.0 g starch, 4.0 g yeast extract, 2.0 g peptone, 18.0 g agar, 1 l filtered seawater). Each strain was then cultured in liquid A1 medium for 7 days while shaking at 230 r.p.m. (25 °C) and cryopreserved at −80 °C in 20 % (v/v) glycerol.
Both strains were inoculated onto A1 agar, marine agar 2216 (MA; Difco), nutrient agar (Difco), R2A agar (Difco), Czapek–Dox (CD) agar (Difco) and tryptic soy agar (TSA; Mediatech) and incubated at 25 °C for 7 days for morphological studies. The temperature range for growth of strains CNX-216T and CNU-914T was examined from 4 to 45 °C (in 5 °C intervals) on these same media. NaCl requirements were examined on A1 medium (using distilled water instead of filtered seawater) containing NaCl at concentrations from 0 to 15 % (w/v) (in 1 % intervals). Growth at pH 1–11 (in 1 pH unit intervals) was tested in marine broth. Gram staining was performed according to established protocols (Gerhardt, 1981). Anaerobic growth was tested for 7 days at 25 °C on A1 agar and MA in an anaerobic jar. Flexirubin-type pigment production and CM-cellulose hydrolysis were determined as described previously (Bernardet et al., 2002). Casein, agar and starch hydrolysis was determined according to established methods (Smibert & Krieg, 1994), as was chitin hydrolysis (Høvik Hansen & Sørheim, 1991). Catalase activity was determined by assessing bubble production in 3 % (v/v) H2O2 and oxidase activity was determined using a 1 % (w/v) solution of tetramethyl-p-phenylenediamine (Kovács, 1956). Carbohydrate metabolism was investigated using API 50CH test strips (bioMérieux) according to the manufacturer’s recommendations. In addition, API 20E, API 20NE and API ZYM kits (bioMérieux) were used to determine additional biochemical properties.
Fatty acid methyl esters were analysed according to the MIDI/Hewlett Packard Microbial Identification System protocols from biomass generated from strains CNX-216T and CNU-914T grown on MA plates for 72 h at 25 °C. DNA G+C content was determined by HPLC analysis as described previously (Martin et al., 1997). Isoprenoid quinones were extracted and separated by HPLC as described previously (Bligh & Dyer, 1959; Collins & Jones, 1981). Cell motility and morphology were observed using phase-contrast microscopy and scanning electron microscopy. For electron microscopy, samples were prepared according to standard protocols (Collins et al., 1993).
Chromosomal DNA from strains CNX-216T and CNU-914T was isolated using the QIAamp DNA Mini kit (Qiagen). 16S rRNA genes were amplified by PCR using the universal primers 27f and 1492r, purified using the MinElute PCR purification kit (Qiagen) according to the manufacturer’s instructions and sequenced on a Perkin-Elmer capillary sequencer (model ABI 3730XL; Applied Biosystems) using the same primers. The sequences were analysed using the blast algorithm (Altschul et al., 1990) and a multiple sequence alignment of representative sequences was created using clustal w version 1.8 (Thompson et al., 1994). Neighbour-joining and maximum-likelihood trees were generated using mega5 (Tamura et al., 2011).
Strain CNX-216T was isolated from a marine sediment sample collected at a depth of 7 m from Penguin Spit, inside the fringing reef at Palmyra Atoll in the Northern Line Islands. This atoll is more than 1600 km from Hawaii and represents one of the most remote shallow-water marine ecosystems on Earth. CNX-216T is a Gram-negative, aerobic, non-motile, rod-shaped bacterium. It forms dark-orange, rounded colonies on A1 agar and MA at 25 °C and produces umbonate colonies with lobate margins on nutrient agar and R2A agar. It grows well between 20 and 40 °C, with an optimal temperature of 30 °C. The strain did not grow at 4–15 or 45 °C on any media and only grew on nutrient agar and medium R2A at 20–30 °C. No growth was observed on CD agar or TSA at any temperature. Moreover, colonies were detected on medium prepared with 0–8 % NaCl but not at higher NaCl concentrations. Growth of strain CNX-216T was observed at pH 5–8 but not at pH 1–4 or 9–11.
The 16S rRNA gene sequence of strain CNX-216T (1424 bp) was analysed using the blast algorithm. CNX-216T shares the closest sequence identity with Cesiribacter roseus 311T (87.1 %) (Liu et al., 2012), C. andamanensis AMV16T (86.8 %) (Srinivas et al., 2011), Adhaeribacter aerolatus 6515J-31T (86.6 %), A. aerophilus 6424S-25T (85.8 %) (Weon et al., 2010) and Litoribacter ruber YIM CH208T (85.7 %) (Tian et al., 2010). These type strains are members of the families Flammeovirgaceae and Cytophagaceae in the order Cytophagales.
A phylogenetic analysis was performed on the nearly complete 16S rRNA gene sequences of strains CNX-216T and CNU-914T. The 71 reference sequences used in the analysis include at least one type strain from each family in the order Cytophagales, representative top blast matches and four uncharacterized but morphologically similar bacterial strains (CNU-893, CNU-916, CNX-520 and CUA-287) that were isolated from marine sediments using the same methods that yielded strains CNX-216T and CNU-914T. Strain CNX-216T forms a deeply branching sister lineage with CNU-914T, ‘Porifericola rhodea’ N5EA6-3A2B, ‘Tunicatimonas pelagia’ N5DB8-4 and the four uncharacterized marine strains (Fig. 1). The most closely related type strains are in the family Flammeovirgaceae (C. roseus 311T and C. andamanensis AMV16T); however, the tree clearly places CNX-216T in a distinct phylogenetic lineage.
Fig. 1.
Neighbour-joining phylogenetic tree based on 16S rRNA gene sequences (1335 bp), showing relationships between strains CNX-216T and CNU-914T and representatives from related families in the phylum Bacteroidetes. Bootstrap values ≥50 % (from 1000 replicates) from neighbour-joining/maximum-likelihood analyses are shown at nodes. Filled circles indicate nodes that were observed with both neighbour-joining and maximum-likelihood algorithms. Type strains outside of the Cytophagales were used as an outgroup. Bar, 0.02 substitutions per nucleotide position.
Strain CNX-216T exhibits many different characteristics in comparison with the most closely related type strains (Table 1). It is the only strain to have originated from a marine source, suggesting major habitat differences. Other differences include DNA G+C content and β-galactosidase and α-fucosidase activities. The whole-cell fatty acid composition of strain CNX-216T was also very different from those of related strains and included at least one unknown (ECL 14.959) that was unique to this strain (Table 2). The major cellular fatty acids were C16 : 1ω5c (32.4 %), iso-C15 : 0 (20.0 %), summed feature 4 (anteiso-C17 : 1 B and/or iso-C17 : 1 I; 17.5 %) and iso-C17 : 0 3-OH (10.3 %). Based on its phylogenetic divergence and distinct characteristics, we propose that strain CNX-216T belongs to a novel family-level taxonomic group within the phylum Bacteroidetes, Mooreiaceae fam. nov.
Table 1. Characteristics of strain CNX-216T and related type strains.
Strains: 1, CNX-216T; 2, C. roseus 311T (data from Liu et al., 2012); 3, C. andamanensis AMV16T (Srinivas et al., 2011); 4, A. aerolatus 6515J-31T (Weon et al., 2010); 5, A. aerophilus 6424S-25T (Weon et al., 2010); 6, L. ruber YIM CH208T (Tian et al., 2010). nr, Not reported. Cells of all strains are rods.
| Characteristic | 1 | 2 | 3 | 4 | 5 | 6 |
| Source | Sediment | Desert sand | Volcanic soil | Air | Air | Soda lake |
| Motility | − | + | − | − | − | − |
| Ranges for growth | ||||||
| NaCl (%, w/v) | 0–8 | 0–3 | 0–5 | 0–1.5 | 0–1 | 0–9 |
| pH | 5–8 | 7–10 | 6–8 | 6.5–9.0 | 6.5–8.5 | 7.5–10.5 |
| Temperature for growth (°C) | ||||||
| Range | 20–40 | 4–37 | 18–37 | 10–35 | 10–37 | 20–37 |
| Optimum | 30 | 30 | 30–37 | nr | nr | 28 |
| Nitrate reduction to nitrite | − | + | + | − | − | + |
| Hydrolysis of: | ||||||
| Gelatin | + | + | − | + | + | − |
| Starch | + | + | − | + | + | + |
| DNA G+C content (mol%) | 57.7 | 47.1 | 50.9 | 43.9 | 44.5 | 45.1 |
| Major quinone | MK-7 | MK-7 | MK-4 | MK-7 | MK-7 | MK-7 |
| Enzyme activities | ||||||
| β-Galactosidase | + | − | nr | − | − | − |
| α-Fucosidase | + | − | nr | − | − | − |
Table 2. Cellular fatty acid profiles of strain CNX-216T and related strains.
Strains: 1, CNX-216T; 2, C. roseus 311T (data from Liu et al., 2012); 3, C. andamanensis AMV16T (Srinivas et al., 2011); 4, A. aerolatus 6515J-31T (Weon et al., 2010); 5, A. aerophilus 6424S-25T (Weon et al., 2010); 6, L. ruber YIM CH208T (Tian et al., 2010). Values are percentages of the total fatty acids. −, Not detected/no data reported; tr, trace (<1 %).
| Fatty acid | 1 | 2 | 3 | 4 | 5 | 6 |
| Straight | ||||||
| C12 : 0 | − | − | 7.0 | − | − | − |
| C14 : 0 | 0.5 | − | − | − | − | − |
| C16 : 0 | 0.5 | 3.7 | 2.6 | 1.8 | 1.7 | 1.8 |
| C18 : 0 | 0.2 | 3.7 | − | − | − | − |
| Branched | ||||||
| iso-C13 : 0 | − | tr | − | − | − | − |
| iso-C15 : 0 | 20.0 | 21.9 | 14.4 | 15.0 | 19.1 | − |
| iso-C16 : 0 | 0.4 | − | − | − | 0.3 | 1.7 |
| iso-C17 : 0 | 2.0 | 3.2 | − | 1.6 | 1.8 | 2.5 |
| iso-C18 : 0 | 0.2 | − | − | − | − | − |
| iso-C19 : 0 | − | − | 9.7 | − | − | − |
| iso-C15 : 1 | − | 4.0 | − | − | − | − |
| iso-C15 : 1 G | − | − | 15.9 | − | − | 3.0 |
| iso-C16 : 1 G | − | − | 11.1 | − | − | − |
| iso-C16 : 1 H | − | − | − | 0.4* | 0.4* | 1.7 |
| iso-C17 : 1ω9c | − | − | − | 0.6 | − | 19.9 |
| anteiso-C11 : 0 | − | − | 5.4 | − | − | − |
| anteiso-C12 : 0 | − | − | 4.1 | − | − | − |
| anteiso-C15 : 0 | 0.2 | − | 3.4 | 1.3 | 1.3 | 4.7 |
| anteiso-C16 : 0 | − | − | 3.0 | − | − | − |
| anteiso-C17 : 0 | 0.6 | − | 3.7 | 0.4 | 0.6 | − |
| Unsaturated | ||||||
| C13 : 1 | − | − | 13.8 | − | − | − |
| C15 : 1ω6c | − | − | − | − | 0.7 | 3.1 |
| C16 : 1ω5c | 32.4 | 29.9 | − | 17.4 | 11.3 | 6.5 |
| C17 : 1ω6c | 1.6 | − | − | 1.3 | 3.6 | 8.7 |
| C17 : 1ω8c | − | − | − | − | − | 1.6 |
| C18 : 1ω7c | − | 1.2 | − | − | − | − |
| C18 : 1ω8c | − | − | − | 0.6 | − | − |
| C18 : 1ω9c | − | 1.3 | − | − | − | − |
| Hydroxy | ||||||
| C15 : 0 3-OH | − | − | − | − | − | 12.1 |
| C16 : 0 2-OH | − | − | − | 0.4 | − | − |
| C16 : 0 3-OH | 0.4 | − | − | 0.3 | − | 0.8 |
| C17 : 0 2-OH | − | − | − | − | − | 0.4 |
| C17 : 0 3-OH | 0.4 | − | − | − | − | − |
| iso-C13 : 0 3-OH | − | 1.1 | − | − | − | − |
| iso-C15 : 0 3-OH | 1.7 | 3.1 | − | 2.9 | 2.9 | 4.1 |
| iso-C16 : 0 3-OH | 0.5 | − | − | 0.5 | 0.6 | 0.5 |
| iso-C17 : 0 3-OH | 10.3 | 13.3 | − | 6.2 | 8.7 | 11.3 |
| Unknown | ||||||
| ECL 11.543 | 0.2 | − | − | 0.8 | 0.6 | − |
| ECL 13.565 | 2.4 | − | − | 3.6 | 3.3 | − |
| ECL 14.959 | 3.0 | − | − | − | − | − |
| ECL 16.582 | 1.4 | − | − | 0.7 | 0.8 | − |
| ECL 18.814 | − | − | − | − | 0.3 | − |
| Summed features† | ||||||
| 1 | − | − | − | 0.4 | 0.6 | − |
| 2 | 0.1 | − | − | − | − | − |
| 3 | 0.5 | 1.2 | − | 14.2 | 8.4 | 10.7 |
| 4 | 17.5 | 13.0 | − | 29.9 | 33.1 | − |
| 5 | 3.2 | − | 5.9 | − | − | − |
Cited as ‘iso-C16 : 0 H’ by Weon et al. (2010). This may be a typographical error.
Summed features represent groups of two or three fatty acids that could not be separated by GLC with the MIDI system. Summed feature 1 contains C13 : 0 3-OH and/or iso-C15 : 1 H; summed feature 2 contains C14 : 0 3-OH and/or iso-C16 : 1 I; summed feature 3 contains C16 : 1ω7c and/or iso-C15 : 0 2-OH; summed feature 4 contains anteiso-C17 : 1 B and/or iso-C17 : 1 I; summed feature 5 contains anteiso-C18 : 0 and/or C18 : 2ω6,9c.
Strain CNU-914T was isolated from a marine sediment sample collected at a depth of 8 m off Parson’s Landing, Catalina Island, CA, USA. It is a Gram-negative, aerobic, motile bacterium that forms short, curved rods and rounded, pink colonies at 20–35 °C on A1 agar and MA. CNU-914T failed to grow on nutrient agar, R2A agar, CD agar or TSA. The optimal growth temperature was 30 °C, while no growth was observed at 4–15 or 40–45 °C. Colony formation was observed on media prepared with 1–5 % NaCl but not in the absence of NaCl or in 6–15 % NaCl. Growth of strain CNU-914T was observed at pH 6–8 but not at pH 1–5 or 9–11.
blast analysis of the 16S rRNA gene sequence of CNU-914T (1425 bp) revealed that it was most similar to Roseivirga spongicola UST030701-084T (88.2 % identity) (Lau et al., 2006), R. ehrenbergii KMM 6017T (87.6 %) (Nedashkovskaya et al., 2005a), R. echinicomitans KMM 6058T (87.0 %) (Nedashkovskaya et al., 2005b) and Fabibacter halotolerans UST030701-097T (87.0 %) (Lau et al., 2006). All of these species belong to the family Flammeovirgaceae in the phylum Bacteroidetes. Closer sequence similarities were observed with strains for which the names ‘P. rhodea’ N5EA6-3A2B (97.6 % similarity) and ‘T. pelagia’ N5DB8-4 (88.8 %) have been proposed. Phylogenetic analysis placed CNU-914T in a well-supported clade that includes ‘P. rhodea’ N5EA6-3A2B, ‘T. pelagia’ N5DB8-4 and the uncharacterized marine strains CNU-287, CNU-893, CNU-916 and CNX-520 (Fig. 1). This clade is sister to the deeply branching CNX-216T sequence and is made up entirely of marine-derived strains.
Strain CNU-914T displays a number of subtle differences from related type strains in the family Flammeovirgaceae, including a narrower temperature tolerance and slightly higher DNA G+C content (Table 3). With regard to cellular fatty acid composition, strain CNU-914T possesses many differences, including five unique straight-chain fatty acids and four unique unsaturated fatty acids (Table 4). CNU-914T also possesses four unknown fatty acids. Strain CNU-914T, ‘P. rhodea’ N5EA6-3A2B and ‘T. pelagia’ N5DB8-4, which form a distinct clade in the phylogenetic tree, all contain iso-C15 : 0, C16 : 1ω5c and iso-C17 : 0 3-OH as major fatty acids. The type strains that fall outside of this lineage differ in that they contain iso-C15 : 1 and not C16 : 1ω5c as a major fatty acid. Based on its phylogenetic position and distinct characteristics, we propose that strain CNU-914T belongs to a novel family-level taxonomic group, Catalimonadaceae fam. nov.
Table 3. Characteristics of strain CNU-914T and related strains.
Strains: 1, CNU-914T; 2, ‘P. rhodea’ N5EA6-3A2B (data from Yoon et al., 2011a); 3, ‘T. pelagia’ N5DB8-4 (Yoon et al., 2012); 4, R. spongicola UST030701-084T (Lau et al., 2006); 5, R. ehrenbergii KMM 6017T (Nedashkovskaya et al., 2005a); 6, R. echinicomitans KMM 6058T (Nedashkovskaya et al., 2005b); 7, F. halotolerans UST030701-097T (Lau et al., 2006). (+), Weakly positive; nr, not reported. All strains contain MK-7 as the major quinone, are positive for catalase and are negative for hydrolysis of agar.
| Characteristic | 1 | 2 | 3 | 4 | 5 | 6 | 7 |
| Source | Sediment | Sponge | Sea anemone | Sponge | Sea water | Sea urchin | Sponge |
| Pigmentation | Pink | Red/pink | Red/pink | Pink | Orange | Pink | Pink |
| Cell morphology | Short curved rods | Straight rods | Straight rods | Straight rods | Rods | Rods | Short curved rods |
| Gliding motility | + | − | − | + | + | − | + |
| Ranges for growth | |||||||
| Temperature (°C) | 20–35 | 15–37 | 20–37 | 12–44 | 4–40 | 4–31 | 12–36 |
| NaCl (%, w/v) | 1–5 | 1–10 | 1–8 | 0–16 | 5.5–8 | 4–8 | 0–12 |
| pH | 6–8 | 6–9 | 6–10 | 5–10 | 5.5–8 | nr | 5–10 |
| Flexirubin | − | − | − | − | + | − | − |
| Nitrate reduction | − | − | − | − | − | + | − |
| Oxidase | + | − | − | + | + | + | + |
| Hydrolysis of: | |||||||
| Gelatin | − | + | − | + | − | + | − |
| Starch | − | − | − | − | − | − | (+) |
| DNA G+C content (mol%) | 44.4 | 43.0 | 52.6 | 43.7 | 40.3 | 41.3 | 42.5 |
Table 4. Cellular fatty acid profiles for strain CNU-914T and related strains.
Strains: 1, CNU-914T; 2, ‘P. rhodea’ N5EA6-3A2B (data from Yoon et al., 2011a); 3, ‘T. pelagia’ N5DB8-4 (Yoon et al., 2012); 4, R. spongicola UST030701-084T (Lau et al., 2006); 5, R. ehrenbergii KMM 6017T (Nedashkovskaya et al., 2005a); 6, R. echinicomitans KMM 6058T (Nedashkovskaya et al., 2005b); 7, F. halotolerans UST030701-097T (Lau et al., 2006). Values are percentages of total fatty acids. nr, Not recorded; −, not detected; tr, trace (<1 %).
| Fatty acid | 1 | 2 | 3 | 4 | 5 | 6 | 7 |
| Straight | |||||||
| C12 : 0 | 0.03 | nr | nr | − | nr | nr | − |
| C14 : 0 | 0.5 | nr | nr | − | nr | nr | − |
| C15 : 0 | 1.2 | nr | nr | − | 1.1 | nr | − |
| C16 : 0 | 1.0 | nr | nr | − | nr | nr | − |
| C17 : 0 | 0.6 | nr | nr | − | nr | nr | − |
| C18 : 0 | 0.3 | nr | nr | − | nr | nr | − |
| Branched | |||||||
| iso-C13 : 0 | 0.1 | nr | 9.8 | 0.7 | 5.2 | 2.9 | 1.6 |
| iso-C14 : 0 | − | 1.0 | tr | − | nr | 1.9 | 4.7 |
| iso-C15 : 0 | 26.8 | 34.4 | 24.5 | 18.6 | 33.5 | 20.2 | 18.3 |
| iso-C16 : 0 | 0.4 | 1.2 | − | 2.0 | 1.2 | 1.8 | 1.2 |
| iso-C17 : 0 | 0.6 | nr | nr | − | nr | 1.0 | 0.5 |
| iso-C15 : 1 | − | nr | nr | 12.5 | 20.5 | 20.2 | 14.2 |
| iso-C16 : 1 | − | nr | nr | − | nr | 2.0 | 1.2 |
| iso-C15 : 1 G | 5.8 | 4.9 | 11.3 | − | nr | nr | − |
| iso-C16 : 1 G | 0.1 | nr | nr | − | nr | nr | − |
| iso-C17 : 1ω9c | − | nr | nr | 10.8 | nr | 1.1 | − |
| anteiso-C15 : 0 | 5.2 | 7.4 | − | 12.5 | 2.4 | 13.1 | 2.5 |
| anteiso-C15 : 1 | − | nr | nr | − | nr | 2.4 | 0.8 |
| anteiso-C17 : 0 | 0.2 | nr | nr | − | nr | nr | − |
| Unsaturated | |||||||
| C13 : 1 at 12–13 | 0.2 | nr | nr | − | nr | nr | − |
| C14 : 1ω5c | 0.1 | nr | nr | − | nr | nr | − |
| C15 : 1ω8c | 0.2 | nr | nr | − | nr | nr | − |
| C16 : 1ω5c | 22.6 | 17.5 | 21.3 | − | nr | nr | − |
| C17 : 1ω6c | 1.2 | nr | nr | − | nr | nr | − |
| Hydroxy | |||||||
| C12 : 0 2-OH | 0.1 | nr | nr | − | nr | nr | − |
| C15 : 0 2-OH | 0.7 | nr | nr | 3.2 | nr | nr | 1.9 |
| C15 : 0 3-OH | − | nr | nr | − | nr | nr | 1.3 |
| C16 : 0 3-OH | 1.8 | 1.9 | 3.2 | − | 1.8 | 1.4 | 1.2 |
| C17 : 0 2-OH | 0.5 | nr | nr | 10.1 | nr | 2.0 | 1.3 |
| C17 : 0 3-OH | 0.4 | nr | nr | − | nr | nr | − |
| iso-C14 : 0 3-OH | 0.2 | nr | nr | − | nr | nr | 1.1 |
| iso-C15 : 0 3-OH | 4.4 | 3.4 | 5.1 | 4.9 | 5.6 | 4.1 | 12.5 |
| iso-C16 : 0 3-OH | 0.4 | 1.0 | − | 1.2 | 7.2 | 4.2 | 12.7 |
| iso-C17 : 0 3-OH | 12.0 | 12.4 | 9.8 | 18.3 | 11.2 | 12.1 | 9.3 |
| Unknown | |||||||
| ECL 11.543 | 0.3 | nr | nr | − | nr | nr | − |
| ECL 13.565 | 1.4 | nr | nr | − | nr | nr | − |
| ECL 14.959 | 5.6 | nr | nr | − | nr | nr | − |
| ECL 16.582 | 1.2 | nr | nr | − | nr | nr | − |
| Unidentified | 5.3 | ||||||
| Summed features* | |||||||
| 2 | 0.4 | nr | nr | − | nr | nr | − |
| 3 | 2.4 | 2.7 | 5.3 | 5.5 | 4.8 | 1.0 | 13.7 |
| 4 | 1.2 | 1.2 | − | − | nr | nr | − |
| 5 | 0.1 | nr | nr | − | nr | nr | − |
Summed features represent groups of two or three fatty acids that could not be separated by GLC with the MIDI system. Summed feature 2 contains C14 : 0 3-OH and/or iso-C16 : 1 I; summed feature 3 contains C16 : 1ω7c and/or iso-C15 : 0 2-OH; summed feature 4 contains anteiso-C17 : 1 B and/or iso-C17 : 1 I; summed feature 5 contains anteiso-C18 : 0 and/or C18 : 2ω6,9c.
The proposed family Catalimonadaceae fam. nov. currently comprises the genus Catalinimonas only; however, the proposed taxa ‘Porifericola’ (Yoon et al., 2011b) and ‘Tunicatimonas’ (Yoon et al., 2012), as well as a number of uncharacterized strains, fall within this family (Fig. 1). Collectively, the families Catalimonadaceae fam. nov. and Mooreiaceae fam. nov. split the Flammeovirgaceae into two clades. One clade has strong bootstrap support and includes the type strain of the type species of the type genus of the family (Flammeovirga aprica NBRC 15941T), suggesting that the family should be limited to this lineage. The second lineage is not well supported and includes Roseivirga and six other genera. This lineage may warrant taxonomic revision.
Despite the phylogenetic and phenotypic differences between strains CNX-216T and CNU-914T, they both produce related alkaloid secondary metabolites (results not shown). This is not a unique observation within the phylum Bacteroidetes, as the marine gliding bacterium Rapidithrix thailandica (Srisukchayakul et al., 2007) and the non-motile species Ohtaekwangia kribbensis (Yoon et al., 2011b) have both been reported to produce the alkaloid marinoquinoline A (Okanya et al., 2011; Sangnoi et al., 2008), which is structurally similar to compounds produced by strain CNX-216T. Remarkably, these alkaloid-producing strains are all marine-derived and belong to as many as three different families within the phylum Bacteroidetes, suggesting that the production of these compounds is highly conserved and may represent an adaptation to survival in marine habitats.
Description of Mooreia gen. nov.
Mooreia (Moore′i.a. N.L. fem. n. Mooreia named after the Gordon and Betty Moore Foundation).
Cells are Gram-negative, aerobic, non-motile and rod-shaped (Fig. S1, available in IJSEM Online). Oxidase and catalase are positive. Nitrate is not reduced. Acid is not produced from glucose fermentation. NaCl is not required for growth. Flexirubin-type pigments are absent. The predominant fatty acids are C16 : 1ω5c, iso-C15 : 0, summed feature 4 (anteiso-C17 : 1 B and/or iso-C17 : 1 I) and iso-C17 : 0 3-OH. MK-7 is the predominant respiratory quinone. Phylogenetically, the genus belongs to the family Mooreiaceae fam. nov. in the order Cytophagales. The type species of the genus is Mooreia alkaloidigena.
Description of Mooreia alkaloidigena sp. nov.
Mooreia alkaloidigena [al.ka.loi.di′ge.na. N.L. n. alkaloidum alkaloid; L. fem. suff. -gena (from L. v. gigno to produce) producing; N.L. fem. adj. alkaloidigena producing alkaloids].
Main characteristics are as given for the genus. In addition, cells are 0.5–0.7 µm wide and 2–3 µm long. Colonies are circular, convex and deep orange on A1 medium, MA, nutrient agar and TSA. On nutrient agar and R2A agar at 20–30 °C, umbonate colonies with a lobate margin are observed. Grows at 20–40 °C with an optimum temperature of 30 °C. The DNA G+C content of the type strain is 57.7 mol%. Tolerates 0–8 % NaCl (w/v) and grows at pH 5–10. Tryptophan deaminase activity is not present. Indole and H2S are not produced. The Voges–Proskauer reaction is negative. Starch, CM-cellulose, chitin, agar, chitosan, aesculin and gelatin are hydrolysed. Casein is hydrolysed weakly. Alkaline phosphatase, esterase (C4), esterase lipase (C8), leucine arylamidase, valine arylamidase, cystine arylamidase, trypsin, α-chymotrypsin, acid phosphatase, naphthol-AS-BI-phosphohydrolase, α-galactosidase, β-galactosidase, α-glucosidase, N-acetyl-β-glucosaminidase and α-fucosidase activities are positive. No activities are detected for lipase (C14), β-glucuronidase, β-glucosidase, α-mannosidase, arginine dihydrolase, lysine decarboxylase, ornithine decarboxylase or urease. Produces acid from d-xylose, d-galactose, d-glucose, d-fructose, d-mannose, methyl α-d-mannopyranoside, methyl α-d-glucopyranoside, N-acetylglucosamine, amygdalin, arbutin, aesculin, salicin, cellobiose, maltose, lactose, melibiose, sucrose, trehalose, inulin, melezitose, raffinose, turanose, d-lyxose, d-tagatose and d- and l-fucose. A positive reaction is observed for β-galactosidase (substrate 4-nitrophenyl β-d-galactopyranoside) and negative reactions are observed for glucose fermentation, arginine dihydrolase and urease in API 20NE test strips. Does not assimilate d-glucose, l-arabinose, d-mannose, d-mannitol, N-acetylglucosamine, maltose, potassium gluconate, capric acid, adipic acid, malic acid, trisodium citrate or phenylacetic acid. API 20E tests show positive reactions for β-galactosidase (substrate 2-nitrophenyl β-d-galactopyranoside) and negative reactions for arginine dihydrolase, lysine decarboxylase, ornithine decarboxylase, citrate utilization and oxidation of mannitol, inositol, sorbitol and rhamnose. Based on API 50CH and API 20NE tests, unable to utilize the following carbon sources for growth or acid production: glycerol, erythritol, d- and l-arabinose, d-ribose, l-xylose, d-adonitol, methyl β-d-xylopyranoside, d-glucose, l-sorbose, l-rhamnose, dulcitol, inositol, d-mannitol, d-sorbitol, starch, glycogen, xylitol, gentiobiose, d- and l-arabitol, potassium gluconate and potassium 2- and 5-ketogluconate.
The type strain, CNX-216T ( = DSM 25187T = KCCM 90102T), was isolated from a marine sediment sample collected at the Palmyra Atoll in the Northern Line Islands in the US Minor Outlying Islands.
Description of Mooreiaceae fam. nov.
Mooreiaceae (Moore.i.a.ce′a.e. N.L. fem. n. Mooreia type genus of the family; suff. -aceae ending to denote a family; N.L. fem. pl. n. Mooreiaceae the family of the genus Mooreia).
Falls is within the order Cytophagales and encompasses Gram-negative bacteria retrieved from marine samples. Currently, the family comprises only the genus Mooreia. The delineation of the family is determined primarily from the phylogenetic position of the 16S rRNA gene sequence. The detailed description is the same as that given for the genus Mooreia. The type genus of the family is Mooreia.
Description of Catalinimonas gen. nov.
Catalinimonas (Ca.ta.li.ni.mo′nas. N.L. n. Catalina Catalina Island in the Channel Islands, CA, USA; L. fem. n. monas a unit, monad; Catalinimonas a monad from Catalina Island, referring to the isolation of the type strain of the type species).
Cells are Gram-negative, aerobic, motile, short, curved rods (Fig. S2). Oxidase and catalase are positive. NaCl is required for growth. Nitrate is not reduced. Acid is produced (weakly) from glucose fermentation. Flexirubin-type pigments are absent. The major respiratory quinone is MK-7. The predominant fatty acids are iso-C15 : 0, C16 : 1ω5c and iso-C17 : 0 3-OH. The type species is Catalinimonas alkaloidigena.
Description of Catalinimonas alkaloidigena sp. nov.
Catalinimonas alkaloidigena [al.ka.loi.di.ge′na. N.L. n. alkaloidum alkaloid; L. fem. suff. -gena (from L. v. gigno to produce) producing; N.L. fem. adj. alkaloidigena producing alkaloids].
Main characteristics are as given for the genus. The DNA G+C content of the type strain is 44.4 mol%. Pink-pigmented colonies are formed on A1 medium and MA. Growth is observed at 15–30 °C and is optimal at 25 °C. Growth is not observed at 4–15, 40 or 45 °C. No growth is detected at NaCl concentrations higher than 9 % (w/v). Grows at pH 5–10 but not at pH 4. Arginine dihydrolase, lysine decarboxylase, ornithine decarboxylase and tryptophan deaminase activities are not present. H2S, urease, indole and acetone are not produced. Aesculin is hydrolysed but starch, casein, agar, chitin, chitosan, CM-cellulose and gelatin are not hydrolysed. API ZYM assays reveal activities of alkaline phosphatase, esterase (C4), esterase lipase (C8), leucine arylamidase, valine arylamidase, cystine arylamidase, α-chymotrypsin, acid phosphatase, naphthol-AS-BI-phosphohydrolase and N-acetyl-β-glucosaminidase. Lipase (C14), trypsin, α-galactosidase, β-galactosidase, β-glucuronidase, α-glucosidase, β-glucosidase, α-mannosidase and α-fucosidase activities are not detected in API ZYM tests. In API 50CH test strips, acid is produced from d-mannose, inositol, aesculin and d-glucose (weakly). In API 20NE test strips, positive reactions are observed for β-glucosidase hydrolysis and β-galactosidase (substrate 4-nitrophenyl β-d-galactopyranoside). Assimilates l-arabinose, d-mannose, N-acetylglucosamine, maltose, potassium gluconate, trisodium citrate and phenylacetic acid but not d-glucose, d-mannitol, capric acid, adipic acid or malic acid. In API 20E tests, a positive reaction is detected for gelatinase and negative reactions are detected for β-galactosidase, citrate utilization and oxidation of mannitol, inositol, sorbitol, rhamnose and arabinose. Based on API 50CH and API 20NE test results, unable to utilize the following carbon sources for growth or acid production: glycerol, erythritol, d- and l-arabinose, d-ribose, d- and l-xylose, d-adonitol, methyl β-d-xylopyranoside, d-galactose, d-fructose, l-sorbose, l-rhamnose, dulcitol, d-mannitol, d-sorbitol, methyl α-d-mannopyranoside, methyl α-d-glucopyranoside, N-acetylglucosamine, amygdalin, arbutin, salicin, cellobiose, maltose, lactose, melibiose, sucrose, trehalose, inulin, melezitose, raffinose, starch, glycogen, xylitol, gentiobiose, turanose, d-lyxose, d-tagatose, d- and l-fucose, d- and l-arabitol, potassium gluconate and potassium 2- and 5-ketogluconate.
The type strain is CNU-914T ( = DSM 25186T = KCCM 90101T), isolated from a marine sediment sample collected off Catalina Island in the Channel Islands, CA, USA.
Description of Catalimonadaceae fam. nov.
Catalimonadaceae (Ca.ta.li.mo.na.da.ce′a.e. N.L. fem. n. Catalinimonas type genus of the family; suff. -aceae ending to denote a family; N.L. fem. pl. n. Catalimonadaceae the family of the genus Catalinimonas.
Falls within the order Cytophagales and encompasses a group of Gram-negative marine bacteria that until quite recently had only been observed in culture-independent studies. The delineation of the family is primarily recognized by 16S rRNA gene sequence phylogeny, which reveals a deeply branching and well-supported clade that is sister to the proposed family Mooreiaceae. The detailed description of the family Catalimonadaceae is the same as that given for the genus Catalinimonas. The type genus of the family is Catalinimonas.
Acknowledgements
This study was supported by the National Institutes of Health grants 1R01GM086261 (to P. R. J.) and 1R37CA044848 (to W. F.). Research in Palmyra was performed under USFWS Special Use Permit #12533-09021. We are grateful to J. P. Euzéby for help with nomenclature and the Nature Conservancy and the personnel who run the Palmyra Atoll research station for facilitating the fieldwork. Special acknowledgement is given to the Gordon and Betty Moore Foundation for their support of the Palmyra Atoll Research Station.
Footnotes
Two supplementary figures are available with the online version of this paper.
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