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Int J Syst Evol Microbiol 55 (2005), 673-679; DOI  10.1099/ijs.0.02892-0
© 2005 International Union of Microbiological Societies

Marichromatium indicum sp. nov., a novel purple sulfur gammaproteobacterium from mangrove soil of Goa, India

K. Arunasri1, C. Sasikala1, C. V. Ramana2, J. Süling3 and J. F. Imhoff3

1 Environmental Microbial Biotechnology Laboratory, Center for Environment, Institute of Science and Technology, J.N.T. University, Kukatpally, Hyderabad 500 072, India
2 Department of Plant Sciences, School of Life Sciences, University of Hyderabad, PO Central University, Hyderabad 500 046, India
3 Institut für Meereskunde, Abteilung Marine Mikrobiologie, Düsternbrooker Weg 20, 24105 Kiel, Germany

Correspondence
C. Sasikala
sasi449{at}yahoo.ie or
r449{at}sify.com


   ABSTRACT
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A reddish-brown bacterium was isolated from photoheterotrophic enrichments of mangrove soil from the western coast of India, in a medium that contained 10 % (w/v) NaCl. Phylogenetic analysis on the basis of 16S rRNA gene sequences showed that strain JA100T clusters with species of the genus Marichromatium of the class ‘Gammaproteobacteria’. Cells of strain JA100T are Gram-negative, motile rods with monopolar single flagella; they require NaCl, the optimum concentration being 1–4 %, and tolerate concentrations up to 13 %. The strain has vesicular internal membrane structures, bacteriochlorophyll a and, most probably, carotenoids of the spirilloxanthin series. No growth factors are required. A reduced sulfur source is required for growth, and, during growth on reduced sulfur sources as electron donors, sulfur is intermediately deposited as a single large granule within the cell. Strain JA100T could not grow at the expense of other tricarboxylic acid cycle intermediates, except malate. On the basis of 16S rRNA gene sequence analysis and its morphological and physiological characteristics, strain JA100T is sufficiently different from other Marichromatium species to justify its designation as a novel species, for which the name Marichromatium indicum sp. nov. is proposed. The type strain is JA100T (=DSM 15907T=ATCC BAA-741T=JCM 12653T).

Published online ahead of print on 4 October 2004 as DOI 10.1099/ijs.0.02892-0.

The GenBank/EMBL/DDBJ accession number for the 16S rRNA gene sequence of strain JA100T is AJ543328.


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Anoxygenic phototrophic bacteria comprise a number of physiologically and phylogenetically distinct groups, including purple sulfur, purple non-sulfur, green sulfur and green non-sulfur bacteria, heliobacteria and aerobic anoxygenic phototrophic bacteria. Although an ability to perform anoxygenic photosynthesis is shared by all these bacteria, according to 16S rRNA gene sequence data they belong to different major evolutionary lines (Madigan, 2001Go). On the basis of 16S rRNA gene sequence similarity, phototrophic purple bacteria and aerobic bacteria containing bacteriochlorophyll are members of the Proteobacteria, while green sulfur bacteria and green non-sulfur bacteria and heliobacteria represent separate major phylogenetic branches. Purple non-sulfur bacteria belong to the ‘Alphaproteobacteria’ and ‘Betaproteobacteria’, whereas purple sulfur bacteria are members of the ‘Gammaproteobacteria’ (Imhoff, 2001aGo). Marine ecosystems are among the major sources of anoxygenic phototrophic bacteria (Imhoff, 2001bGo), and, in a reclassification of this group, salt requirements were found to be a phenotypic characteristic, in agreement with their phylogenetic relationship (Imhoff et al., 1998Go). In this report, we describe a novel purple sulfur bacterium isolated from mangrove soils from Goa, India. On the basis of phenotypic characteristics and the results of a molecular analysis, the novel isolate is classified as a novel species of the genus Marichromatium, for which the name Marichromatium indicum is proposed.

Strain JA100T was isolated from enrichments of mangrove soils from Goa, India. The medium of Biebl & Pfennig (1981)Go, supplemented with sodium chloride (1 %, w/v), was used. Malate, pyruvate and succinate (each at 0·1 %, w/v) were used as the carbon source and ammonium chloride was used as the nitrogen source and the cultures were grown phototrophically under light (2400 lx) at 30±2 °C. Purification was achieved by means of repeated streaking on agar slants under an argon atmosphere. Purified cultures were grown in completely filled screw-cap test tubes (10x100 mm) for photoheterotrophic growth. Morphological properties (cell shape, cell division, cell size, flagella) were observed by light microscopy (with an Olympus BH-2 microscope). To study the ultrastructure of the flagella, cells were stained with 1 % phosphotungstic acid; ultrathin sections were viewed through a transmission electron microscope (H-7500; Hitachi) to examine intracytoplasmic structures such as the internal membrane system. In vivo absorption spectra were measured with a Spectronic Genesys 2 spectrophotometer using sucrose solution (Trüper & Pfennig, 1981Go). Absorption spectra were also recorded from pigments extracted with acetone after elution of the cell suspension with acetone through a 10x200 mm column packed with aluminium oxide. The utilization of different carbon substrates and electron donors (0·3 %, w/v or v/v, unless otherwise mentioned) was tested in the medium of Biebl & Pfennig (1981)Go containing 5 mM Na2S.9H2O. Nitrogen source (0·12 %, w/v) utilization was tested by replacing ammonium chloride with different nitrogen sources. Diazotrophy of the culture was determined by growth under an N2 atmosphere and was confirmed by repeated subculturing (four times). Growth was measured turbidometrically at 660 nm. Genomic DNA was extracted and purified according to the method of Marmur (1961)Go and the G+C content of the DNA (mol%) was determined by thermal denaturation (Marmur & Doty, 1962Go). Cell material for 16S rRNA gene sequencing was taken from 1–2 ml well-grown liquid cultures. DNA was extracted and purified by using the Qiagen genomic DNA buffer set. PCR amplification and 16S rRNA gene sequencing were done as described previously (Imhoff et al., 1998Go; Imhoff & Pfennig, 2001Go). Sequences were aligned using the CLUSTAL W program (Thompson et al., 1994Go) and the alignment was corrected manually. The distance matrix was calculated using the algorithm of Jukes & Cantor (1969)Go with the DNADIST program within the PHYLIP package (Felsenstein, 1989Go). The FITCH program in the PHYLIP package fitted a tree to the evolutionary distances.

The blackish, subsurface, moist soil sample was collected from mangroves near Goa, India, during May 2001. The area is occasionally flooded by sea water and is also washed by fresh water during the rainy season. During the summer, drying was observed in the area, which may increase the salt concentration of the soil.

Soil samples collected from mangroves were enriched at three different saline concentrations (10, 6 and 0·05 %, w/v) under photoheterotrophic conditions. Purplish-brown enrichments were observed in all the samples after 6 days. Enrichments from the 10 % saline yielded three different colonies in anaerobic agar slants. Under the microscope, cells from one of these, a brown, circular and elevated colony, showed a peculiar cell shape with a single refractile body at the centre of a bloated cell. This isolate, strain JA100T, was used for further studies. The morphology and fine structure of strain JA100T are given in the species description and are shown in Fig. 1Go and Fig. 2Go. A rosette arrangement of cells is very common in both young and old cultures. Transmission electron microscopy of thin sections revealed that strain JA100T possessed vesicular internal membrane structures extending throughout the cell (Fig. 3Go).



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  		Fig. 1. Phase-contrast micrograph of strain JA100T. Arrow indicates globule of elemental sulfur. Bar, 5 µm.

 


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  		Fig. 2. Electron micrograph of negatively stained cells of strain JA100T showing single monopolar monotrichous flagellum. Bar, 1 µm.

 


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  		Fig. 3. Electron micrograph of ultrathin section of strain JA100T showing vesicular nature of photosynthetic membranes extending throughout the cell. Bars, 0·5 µm.

 
In vivo absorption maxima of intact cells (Fig. 4aGo) were recorded at 372, 462, 489, 522, 591, 798 and 852 nm, indicating the presence of bacteriochlorophyll a and carotenoids. Orange/brown-coloured acetone extracts with absorption maxima at 447, 475 and 502 nm (Fig. 4bGo) may indicate the presence of carotenoids of the spirilloxanthin series.



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  		Fig. 4. Whole-cell absorption spectrum (a) of strain JA100T and acetone spectrum (b) of extracted pigments.

 
Strain JA100T was able to grow photolithoautotrophically [anaerobic conditions, in light (2400 lx), with Na2S.9H2O (5 mM) and NaHCO3 (0·1 %, w/v)], photolithoheterotrophically [anaerobic conditions, in light (2400 lx), with Na2S.9H2O (5 mM) and pyruvate (0·3 %, w/v)], photo-organoheterotrophically [anaerobic conditions, in light (2400 lx), with pyruvate (0·3 %, w/v) and cysteine (1 mM)] and chemolithoheterotrophically [microaerobic conditions, in the dark, with thiosulfate (1 mM) and pyruvate (0·3 %, w/v)]. Chemolithoautotrophy could not be demonstrated. The preferred growth mode of strain JA100T was photolithoheterotrophy and photo-organoheterotrophy (only in the presence of cysteine as sulfur source). Strain JA100T could tolerate 8 mM Na2S.9H2O, with an optimal range of 3–6 mM. Sulfide could be replaced with other reduced sulfur compounds such as cysteine, thiosulfate and thioglycollate (Table 1Go). Although feeble growth could be observed in the absence of any reduced sulfur sources, such photo-organoheterotrophic growth was not observed upon repeated subculturing or from old cultures. Replacement of sulfide with cysteine resulted in good biomass yields, which indicates that reduced sulfur compounds may be required for sulfur assimilation in this strain. However, cysteine could not replace reduced inorganic sulfur compounds for photoautotrophic growth (Table 1Go). The organic substrates supporting growth of the strain are given in the species description. Strain JA100T lacks the ability to liquefy gelatin and biotransform tryptophan to indole. Nitrogen sources utilized by JA100T include ammonium chloride, urea and dinitrogen. Those which did not support growth were nitrate, nitrite and glutamate. Strain JA100T has no growth factor requirement. The G+C content of the DNA of strain JA100T was 67·1 mol% (Tm). The sequences of the 16S rRNA genes of strain JA100T, Marichromatium gracile and Marichromatium purpuratum were determined and aligned. Comparative 16S rRNA gene sequence analysis revealed that strain JA100T had the highest levels of similarity to M. gracile and M. purpuratum. These three bacteria formed a cluster separate from other purple sulfur bacteria (Fig. 5Go). This suggests that the novel strain JA100T could be regarded as a representative of the genus Marichromatium.


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  		Table 1. Photolithohetero-/autotrophic growth of strain JA100T on different reduced sulfur sources

Values shown are means of duplicate experiments performed after 48 h light (2400 lx) anaerobic incubation at 30±2 °C in the absence of yeast extract (unless otherwise mentioned). Concentrations used: pyruvate, 0·22 % (w/v); bicarbonate, 0·1 % (w/v); Na2S.9H2O, 5 mM; yeast extract, 1 % (w/v); cysteine, thiosulfate and thioglycollate, all 1 mM. Symbols: +, growth present; –, no growth.

 


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  		Fig. 5. Dendrogram depicting the phylogenetic relationships of strain JA100T within the family Chromatiaceae, determined using 16S rRNA gene sequence analysis. Bar, 1 nucleotide substitution per 100 nucleotides.

 
Improving knowledge of 16S rRNA gene sequence analyses has enabled the phylogenetic relationships of the phototrophic purple sulfur bacteria to be evaluated, and these data were used to initiate a taxonomic reclassification (Imhoff & Süling, 1996Go; Imhoff et al., 1998Go; Guyoneaud et al., 1998Go). One of the proposed reclassifications was the formation of Marichromatium gen. nov. (Imhoff et al., 1998Go) by reclassifying two species of marine purple sulfur bacteria of the genus Chromatium, Chromatium gracile and Chromatium purpuratum. The genus Marichromatium represents true marine purple sulfur bacteria belonging to the class ‘Gammaproteobacteria’, and comprises two well-described species of this genus (the only species known to date), viz. M. gracile and M. purpuratum (Imhoff, 2001aGo). Although the 16S rRNA gene sequence of ‘Rhodobacter marinus’ (Burgess et al., 1994Go) also clusters with those of the genus Marichromatium (Imhoff et al., 1998Go), this bacterial name was never validly published.

In an attempt to isolate marine purple non-sulfur bacteria from mangrove soils of the west coast of India, near Goa, strain JA100T was isolated after enrichment in saline photoheterotrophic media. However, strain JA100T failed to grow under photoheterotrophic conditions [in the absence of sulfide and in the presence of sodium ascorbate (0·05 %, w/v) as reducing agent] upon repeated subculturing in a saline (NaCl at 1 %, w/v) medium. The 16S rRNA gene sequence of strain JA100T clustered with those of the ‘Gammaproteobacteria’ and was found to be most similar to those of the genus Marichromatium, having sequence dissimilarity with M. gracile and M. purpuratum of 3 and 5 %, respectively. Apart from the sequence dissimilarity, strain JA100T has phenotypic variations with respect to these two species (Table 2Go), which justify the description of this strain as a novel species.


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  		Table 2. Differentiating characteristics of species of the genus Marichromatium

Substrates that were utilized by all of the strains include acetate, propionate, butyrate, pyruvate, lactate and malate; those that could not be utilized include caproate, glutamate, glucose, mannitol, glycerol, ethanol, methanol and benzoate. Other similarities of the three strains include rod shape, cell division by binary fission, the presence of a single polar flagellum, vesicular internal membrane structures and the absence of a requirement for a vitamin source. Symbols: +, substrate utilized; –, substrate not utilized; NT, not tested.

 
Although the common habitats of purple sulfur bacteria are the top (anoxic) layers of stratified lakes and shallow aquatic sediments (Van Gemerden & Mas, 1995Go), these organisms are also known to occur in anaerobic and sulfide-containing parts of moist and muddy soils (Pfennig & Trüper, 1989Go), as observed in the case of strain JA100T. Strain JA100T, like other Marichromatium species, has a vesicular type of internal membrane system; this is most common among the Chromatiaceae, with the exception of Thiococcus pfennigii (previously known as Thiocapsa pfennigii; Eimhjellen, 1970Go), Thioalkalicoccus limnaeus (Bryantseva et al., 2000Go) and Thioflavicoccus mobilis (Imhoff & Pfennig, 2001Go), which have a tubular internal membrane system.

Unlike other purple sulfur bacteria, the cells of which usually contain multiple sulfur globules, cells of strain JA100T were always found to contain only one large sulfur globule each. Like all the described species of Marichromatium, strain JA100T also has a requirement for salinity. However, strain JA100T has the lowest salt requirement (0·05 %), and the level of tolerance of NaCl (13 %) in this strain is much higher than that in the others. The observed growth of JA100T in a wide range (0·05–13 %) of salinities reflects its adaptation to its natural habitat, which exhibits different salt concentrations during various seasons. The most obvious difference between strain JA100T and other Marichromatium species is its inability to grow chemoautotrophically (Table 3Go) and its requirement for a reduced sulfur compound as a source of sulfur. Even though the ability to use organic compounds is restricted in purple sulfur bacteria, these organisms are known to metabolize tricarboxylic acid cycle intermediates as carbon sources (Imhoff, 1995Go). However, strain JA100T lacks such an ability, with the exception of malate utilization (Table 3Go). Furthermore, JA100T represents the only species of Marichromatium known to utilize urea as a nitrogen source, though urea-metabolizing representatives are known from other genera of purple sulfur bacteria, i.e. Thiocapsa (Thiocapsa roseopersicina), Thiocystis (Thiocystis violacea) and Allochromatium (a few strains of Allochromatium vinosum) (Bast, 1986Go). In view of the phenotypic and genetic differences between JA100T and its closest relatives in the genus Marichromatium, we propose JA100T as the type strain of a novel species, Marichromatium indicum sp. nov.


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  		Table 3. Phototrophic growth of strain JA100T on various carbon sources

Values shown are means of experiments performed in triplicate after 72 h of light (2400 lx) anaerobic incubation at 30±2 °C. Organic substrates were tested in the presence of Na2S.9H2O (5 mM). Organic substrates were utilized at a concentration of 0·3 % (w/v), except for fatty acids (propionate, butyrate, valerate, caproate), alcohols (ethanol, methanol) and glycerol, which were each used at a concentration of 0·1 % (v/v). Symbols: +, growth present; –, no growth; NA, not applicable.

 
Description of Marichromatium indicum sp. nov.
Marichromatium indicum (in'di.cum. L. neut. adj. indicum named after India, the country in which the type strain was isolated).

Cells are rod-shaped, measuring about 0·8–1·0 µm in width and 2–7 µm in length. Multiply by binary fission and are motile by means of polar flagella. Culture suspension is orange–brown in colour. Internal membranes are of the vesicular type, extending throughout the cell. Pigments include bacteriochlorophyll a and, most probably, carotenoids of the spirilloxanthin series. No requirement for growth factors. Reduced sulfur compounds are obligatory for sulfur assimilation. Growth modes are photolithoheterotrophy and chemolithoheterotrophy, photolithoautotrophy, and photo-organoheterotrophy with cysteine. Organic substrates metabolized include acetate, propionate, butyrate, pyruvate, lactate, malate and fructose; those which cannot be metabolized include valerate, caproate, citrate, fumarate, succinate, tartrate, glutamate, glucose, mannitol, glycerol, ethanol, methanol and benzoate. Ammonium chloride, dinitrogen and urea are the nitrogen sources metabolized. Optimum growth temperature is 30–35 °C, and temperature required for growth is in the range 25–39 °C; pH range is 6·0–7·5. Sodium chloride is required for growth, the optimum being between 1 and 4 % (w/v); 0·05–13 % (w/v) NaCl is tolerated. G+C content of the DNA is 67·1 mol% (Tm).

The habitat of the type strain, JA100T (=DSM 15907T=ATCC BAA-741T=JCM 12653T), is marine mangrove soils.


   ACKNOWLEDGEMENTS
 
Financial assistance received from the Department of Science & Technology (FIST), the Department of Biotechnology and C.S.I.R, Government of India, is acknowledged. The skilful assistance of F. Lappe in preparing DNA, performing sequence analysis and constructing the phylogenetic trees is gratefully acknowledged. Y. Nagamalleshwari and K. Venkatesham of Ruska Labs, ANGR Agricultural University, Hyderabad, are acknowledged for their skilful help with the taking of electron micrographs.


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