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International Journal of Systematic and Evolutionary Microbiology (2015), 65, 2357–2364 DOI 10.1099/ijs.0.000263 Phaeobacterium nitratireducens gen. nov., sp. nov., a phototrophic gammaproteobacterium isolated from a mangrove forest sediment sample Nupur,1 Naga Radha Srinivas Tanuku,2 Takaichi Shinichi3 and Anil Kumar Pinnaka1 Correspondence 1Microbial Type Culture Collection and Gene Bank, CSIR – Institute of Microbial Technology, Anil Kumar Pinnaka Sector 39A, Chandigarh – 160 036, India [email protected] 2CSIR – National Institute of Oceanography, Regional Centre, 176, Lawsons Bay Colony, Visakhapatnam – 530017, India 3Nippon Medical School, Department of Biology, Kosugi-cho, Nakahara, Kawasaki 211-0063, Japan A novel brown-coloured, Gram-negative-staining, rod-shaped, motile, phototrophic, purple sulfur bacterium, designated strain AK40T, was isolated in pure culture from a sediment sample collected from Coringa mangrove forest, India. Strain AK40T contained bacteriochlorophyll a and carotenoids of the rhodopin series as major photosynthetic pigments. Strain AK40T was able to grow photoheterotrophically and could utilize a number of organic substrates. It was unable to grow photoautotrophically and did not utilize sulfide or thiosulfate as electron donors. Thiamine and riboflavin were required for growth. The dominant fatty acids were C12 : 0,C16 : 0, C18 : 1v7c and summed feature 3 (C16 : 1v7c and/or iso-C15 : 0 2-OH). The polar lipid profile of strain AK40T was found to contain diphosphatidylglycerol, phosphatidylethanolamine, phosphatidylglycerol and eight unidentified lipids. Q-10 was the predominant respiratory quinone. The DNA G+C content of strain AK40T was 65.5 mol%. 16S rRNA gene sequence comparisons indicated that the isolate represented a member of the family Chromatiaceae within the class Gammaproteobacteria. 16S rRNA gene sequence analysis indicated that strain AK40T was closely related to Phaeochromatium fluminis, with 95.2 % pairwise sequence similarity to the type strain; sequence similarity to strains of other species of the family was 90.8–94.8 %. Based on the sequence comparison data, strain AK40T was positioned distinctly outside the group formed by the genera Phaeochromatium, Marichromatium, Halochromatium, Thiohalocapsa, Rhabdochromatium and Thiorhodovibrio. Distinct morphological, physiological and genotypic differences from previously described taxa supported the classification of this isolate as a representative of a novel species in a new genus, for which the name Phaeobacterium nitratireducens gen. nov., sp. nov. is proposed. The type strain of Phaeobacterium nitratireducens is AK40T (5JCM 19219T5MTCC 11824T). Mangrove habitats are vital to humankind by virtue of their found in many states of India, including Andhra Pradesh, uses and aesthetic value. They serve as nurseries and feed- the Andaman and Nicobar Islands, Goa, Gujarat, ing and spawning grounds for commercial fin fish and Karnataka, Kerala, Maharashtra, Tamil Nadu and West shellfish. Mangrove habitats are found in locations where Bengal. The significance of microbes in aquatic ecosystems a river enters the sea, and these dynamic ecosystems sup- is well recognized as a result of many pioneer studies port numerous diversified soil microbes. Mangroves are (Longhurst & Harrison, 1989; Wheeler & Kirchman, 1986). Microbes play different roles, including primary producers, secondary producers, consumers and decompo- All authors contributed equally to this study. sers. The activities of these microbes (photosynthetic, litho- The GenBank/EMBL/DDBJ accession number for the 16S rRNA trophic and organotrophic) are important for maintaining T gene sequence of strain AK40 is HF968497. balance in the environment which, in turn, is vital for the Five supplementary figures are available in the online Supplementary maintenance of other life forms. A number of novel bac- Material. terial taxa have been identified from mangrove habitats. 000263 G 2015 IUMS Printed in Great Britain 2357 Nupur and others The family Chromatiaceae was proposed by Bavendamm Preservation was done at (80 8C in modified Pfennig (1924), with the type genus Chromatium, and its description broth with 20 % glycerol. was later emended by Imhoff (1984). Members of the Colony morphology was studied after 72 h of anaerobic Chromatiaceae are Gram-negative, ovoid, rod, spherical, growth of the strain on modified Pfennig medium at spiral or vibrioid-shaped, motile by flagella or non-motile, 30 8C under 2000 lx illumination. The isolated pure multiply by binary fission, may contain gas vesicles and colony was checked for cell morphology and motility by have internal photosynthetic membranes that are of either a using phase-contrast microscopy (Olympus) at 61000 tubular or vesicular type. Cells in the majority of the taxa con- magnification and also by transmission electron micro- tain photosynthetic pigments such as bacteriochlorophyll scope (JEOL JEM 2100) at an operating voltage of (BChl) a or b and carotenoids of the okenone, rhodopinal 200 kV. The Gram reaction was determined by using the or spirilloxanthin groups (Takaichi, 1999). Cultures appear Gram staining kit from HiMedia as described by the in different colours, including orange–brown to brownish manufacturer. red or pink, purple–red and purple–violet, depending on the type of carotenoids present. Cells grow under anoxic con- Physiological and biochemical characteristics were deter- ditions in the presence of light (photolithoautotropically) mined as described previously (Anil Kumar et al., 2008a, with sulfide or sulfur as electron donor and deposit sulfur gran- b; Srinivas et al., 2006). The in vivo absorption spectrum ules within the cells as an intermediate oxidation product that was measured with a Spectronic Genesys 2 spectropho- they may convert to sulfate; and can use hydrogen or tometer in sucrose solution (Tru¨per & Pfennig, 1981). reduced iron as an electron donor and also grow mixotrophi- The absorption spectrum of pigments extracted with cally and photoassimilate a number of organic substrates. acetone was also recorded. Carotenoid composition was Some taxa are also capable of photo-organoheterotrophic analysed by using C18-HPLC (Takaichi & Shimada, 1992). growth. Most members of the Chromatiaceae are strictly Strain AK40T and Phaeochromatium fluminis JA418T were anaerobic and obligately phototrophic, but others grow grown anaerobically on modified Pfennig medium with chemolithoautotrophically or chemo-organoheterotrophically 2 % NaCl at 30 8C under 2000 lx illumination for 3 days under micro-oxic to oxic conditions in the dark. Carbon to prepare fatty acid methyl esters (classical methods) fixation is by the reductive pentose phosphate cycle in all and were analysed using the Sherlock Microbial species tested so far. Several taxa can fix N and store elemen- 2 Identification System (MIDI-6890 with database TSBA50) tal sulfur, poly-b-hydroxybutyrate, polysaccharides and by the protocol described by the manufacturer. At the polyphosphate. Some taxa may require different growth fac- time of harvesting, the cells were in the exponential tors. Members of the Chromatiaceae commonly dwell in phase of growth. Freeze-dried cells were analysed for areas where anoxic conditions prevail with sulfide or sulfur polar lipids and quinones. Cells were extracted for polar sources with illumination, including diverse aquatic habitats lipid analysis (Bligh & Dyer, 1959) and analysed by two- and sediments such as ditches, estuaries, lakes, marine habi- dimensional TLC followed by spraying with appropriate tats, moist and muddy soils, ponds, rivers, salt and soda lakes detection reagents (5 % ethanolic molybdatophosphoric and sulfur springs. The DNA G+C content varies between acid, molybdenum blue, ninhydrin and Molisch reagents) 45.5 and 70.4 mol% (Imhoff, 2005a). (Komagata & Suzuki, 1987). Genomic DNA was isolated In the course of bacterial diversity studies of mangrove by using the procedure of Marmur (1961) and the DNA T samples, a bacterial strain, AK40 , was isolated from a G+C content was determined from melting-point (Tm) mangrove sediment sample collected near Coringa, curves (Sly et al., 1986) obtained by using a Lambda 35 Andhra Pradesh, India. Phylogenetic analysis based on spectrophotometer (Perkin Elmer) equipped with the the 16S rRNA gene sequence revealed that strain AK40T Templab 2.0 software package. was closely related to the genus Phaeochromatium of the For 16S rRNA gene sequencing, DNA was prepared using a family Chromatiaceae. In this study, a polyphasic approach, bacterial DNA isolation kit (Qiagen). The 16S rRNA gene including genotypic, phenotypic and chemotaxonomic was amplified by PCR using universal bacterial primers characterizations, was used to determine the taxonomic 27f (59-AGAGTTTGATCCTGGCTCAG-39) and 1492r position of strain AK40T. (59-TACGGYTACCTTGTTACGACTT-39). The PCR pro- Strain AK40T was isolated from a sediment sample. The duct was purified using a QIA quick PCR purification kit temperature and pH of the sediment sample were 30 8C (Qiagen) and sequenced using an ABI PRISM model and 7.5, respectively. Anoxygenic phototrophic bacterium 3700 automatic DNA sequencer and Big Dye Terminator AK40T was isolated using photolithoheterotrophic enrich- cycle sequencing kit (Applied Biosystems). The 16S rRNA T ments of the sediment sample, and subsequent purification gene sequence of strain AK40 was subjected to BLAST was performed as described previously (Anil Kumar et al., sequence similarity search (Altschul et al., 1990) and
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  • The Eastern Nebraska Salt Marsh Microbiome Is Well Adapted to an Alkaline and Extreme Saline Environment

    The Eastern Nebraska Salt Marsh Microbiome Is Well Adapted to an Alkaline and Extreme Saline Environment

    life Article The Eastern Nebraska Salt Marsh Microbiome Is Well Adapted to an Alkaline and Extreme Saline Environment Sierra R. Athen, Shivangi Dubey and John A. Kyndt * College of Science and Technology, Bellevue University, Bellevue, NE 68005, USA; [email protected] (S.R.A.); [email protected] (S.D.) * Correspondence: [email protected] Abstract: The Eastern Nebraska Salt Marshes contain a unique, alkaline, and saline wetland area that is a remnant of prehistoric oceans that once covered this area. The microbial composition of these salt marshes, identified by metagenomic sequencing, appears to be different from well-studied coastal salt marshes as it contains bacterial genera that have only been found in cold-adapted, alkaline, saline environments. For example, Rubribacterium was only isolated before from an Eastern Siberian soda lake, but appears to be one of the most abundant bacteria present at the time of sampling of the Eastern Nebraska Salt Marshes. Further enrichment, followed by genome sequencing and metagenomic binning, revealed the presence of several halophilic, alkalophilic bacteria that play important roles in sulfur and carbon cycling, as well as in nitrogen fixation within this ecosystem. Photosynthetic sulfur bacteria, belonging to Prosthecochloris and Marichromatium, and chemotrophic sulfur bacteria of the genera Sulfurimonas, Arcobacter, and Thiomicrospira produce valuable oxidized sulfur compounds for algal and plant growth, while alkaliphilic, sulfur-reducing bacteria belonging to Sulfurospirillum help balance the sulfur cycle. This metagenome-based study provides a baseline to understand the complex, but balanced, syntrophic microbial interactions that occur in this unique Citation: Athen, S.R.; Dubey, S.; inland salt marsh environment.