FEMS Microbiology Letters 218 (2003) 359^364


Evidence for limited species diversity of bacteriochlorophyll b-containing purple nonsulfur anoxygenic phototrophs in freshwater habitats
Gerrit J. Hoogewerf, Deborah O. Jung, Michael T. Madigan
Received 8 October 2002; received in revised form 26 November 2002; accepted 26 November 2002 First published online 7 January 2003


Department of Microbiology and Center for Systematic Biology, Southern Illinois University, Carbondale, IL 62901-6508 USA

Thirteen new isolates of bacteriochlorophyll b-containing purple nonsulfur bacteria were isolated from four freshwater habitats using specific enrichment methods including the use of long wavelength filters and extincting dilution of the inoculum. The new isolates were compared with the type strain of Blastochloris viridis, strain DSM 133T , as regards pigments, morphology, carbon nutrition, and phylogeny. All new isolates were budding bacteria, and phototrophic mass cultures were green, brown, or brown^green in color. The pattern of carbon sources photocatabolized were similar in all strains; however, sugars, both mono- and disaccharides, were widely used by the new isolates while they did not support growth of strain DSM 133T . Phylogenetic analysis showed all new strains to cluster tightly with the type strain with the exception of one brown-colored strain and a mildly thermophilic strain. The results suggest that in contrast to purple nonsulfur bacteria containing bacteriochlorophyll a, those containing bacteriochlorophyll b may not be morphologically or phylogenetically diverse, and group into a tight phylogenetic clade distinct from all other anoxygenic phototrophs. ß 2003 Federation of European Microbiological Societies. Published by Elsevier Science B.V. All rights reserved.
Keywords : Anoxygenic phototrophic bacteria ; Purple bacteria; Blastochloris ; Bacteriochlorophyll b

1. Introduction Over 50 species of purple anoxygenic phototrophs have been described and the majority produce bacteriochlorophyll (Bchl) a as their chlorophyll pigment [1]. Within the purple nonsulfur bacteria, only species of the genus Blastochloris (formerly Rhodopseudomonas) [2], contain Bchl b [3^6]. The genus Blastochloris consists of two species, B. viridis and B. sulfoviridis, both nutritionally diverse phototrophs [4,7,8] and excellent nitrogen-¢xers [9,10]. In addition to Blastochloris, four species of purple sulfur bacteria, Halorhodospira halochloris [11], Halorhodospira abdelmaleki [12], Thiococcus pfennigii [13,14], and Thioalkalicoccus limnaeus [15], also produce Bchl b. Thus, of cultured purple bacteria, those containing Bchl b are a distinct minority. We hypothesized that diversity among Bchl b-containing purple nonsulfur bacteria might actually be greater

than currently recognized but that either inherently low population numbers or an inability to compete with Bchl a-containing species bias their development in enrichment cultures. To test this hypothesis we set up a series of enrichment cultures using a light ¢lter that eliminated Bchl a-containing phototrophs. The results of our study, based on the morphology, pigments, carbon nutrition, and phylogeny of 13 new isolates of freshwater Bchl b-containing purple nonsulfur bacteria, indicate that species diversity within this group may indeed be quite low, and that culturable representatives form a tight phylogenetic clade within the alpha Proteobacteria.

2. Materials and methods 2.1. Enrichment and isolation All new isolates of Bchl b-containing phototrophs were obtained from enrichment cultures that employed a light ¢lter (Kodak Wratten Filter 87A) that transmitted less than 1% of wavelengths shorter than 900 nm (Bchl a ab-

* Corresponding author. Tel./Fax : +1 (618) 453 5130. E-mail address : madigan@micro.siu.edu (M.T. Madigan).

0378-1097 / 03 / $22.00 ß 2003 Federation of European Microbiological Societies. Published by Elsevier Science B.V. All rights reserved. doi:10.1016/S0378-1097(02)01195-3

450. brown. 427 422. Carbondale. 604. indicating that populations of Bchl b-containing purple nonsulfur bacteria. yeast extract. USA Crystal Lake Park.1. 832.05%. 603. USA Campus Lake. 604. 452. Ramsey. 452.2.1 g. Monticello. IL. 604. budding rods Brownish-green colonies. budding rods 1014. USA Campus Lake. 833. undiluted inoculum. 0. budding rods Dark green colonies. viridis DSM133T . 50 mg. IL. see Table 1). 604. 0. 604. Hoogewerf et al. A distinct variation in color was obvious in phototrophically grown colonies of the di¡erent isolates. Characterizational studies All isolates were characterized as to their morphology. 0. 452. USA Description Green colonies. 1015. and pigments Enrichment cultures for purple nonsulfur bacteria employing a ¢lter to exclude Bchl a-containing species readily yielded new isolates containing Bchl b from four freshwater habitats (Table 1). Colonies and subsequent phototrophic liquid cultures varied from brown or brown^green to distinctly olive-green in color. Urbana. 400 425. K2 HPO4 . IL. budding rods Dark green colonies. 403 1014. 2. budding rods Green colonies. 483. 483. Growth was monitored turbidimetrically using a KlettSummerson colorimeter (66. budding rods Dark brown colonies. 483. 452. 452. budding rods Light green colonies. cell morphology varied somewhat between strains. 483. IL. Some isolates were obtained from undiluted inocula while others were obtained from extinction culturing of the original inoculum. 452. IL. Carbondale. 452. budding rods Brownish-green colonies. USA Soda Dam hot spring Santa Fe National Forest. 1016. 452. 483. carbon nutrition. 1500 lux at the ¢lter surface. 403 1012. Water or mud^ water slurries were suspended in dilute phosphate bu¡er and transferred to tubes of medium Enrich 1. 604. 451. viridis used in this study Strains Previous isolates DSM 133T (type strain) UN GI New isolatesa G2 (ud) G3 (ud) G5 (ud) G6 (1031 ) G7 (1031 ) G8 (ud) G10 (1032 ) G11 (ud) G12 (ud) B4 (1031 ) B5 (1031 ) B7 (ud) B9 (1031 ) a ously described [18] and approximately 1400 nucleotides were used to generate the phylogenetic tree. 1015. Pure cultures from liquid enrichments were obtained on Petri plates incubated phototrophically in un¢ltered incandescent light. 2. red ¢lter) versus no substrate negative controls. budding rods Brown colonies. 424. Sequence alignments were veri¢ed against the secondary structure of the 16S rRNA gene of B. 423. 400 Brownish-green colonies. USA Allerton Pond. 831. 604. USA Ramsey Lake. 832. IL. 833. Carbon nutrition was determined using medium Enrich 1 in which individual carbon sources were substituted for succinate/acetate/lactate at the concentrations indicated in Table 2.75 g. Urbana. 483. 832. Illumination was from an incandescent spotlight bulb providing ca. NaCl.4 g. 451. 452. 604. sodium acetate. 833. 830. 403 427 422. USA Crystal Lake Park. IL. Absorption spectra were obtained from intact cells suspended in 30% bovine serum albumin. . at least those capable of growth under our enrichment conditions. IL. 833. Medium Enrich 1 contained the following (per liter of distilled water): MgSO4 W7H2 O. 0. 481. 833. New Mexico Crystal Lake Park. medium sized budding rods Dark green colonies. sodium succinate. and phylogeny. KH2 PO4 . maxima (nm) 1014. 832. USA Ramsey Lake. Ramsey. budding rods Brown colonies. 1015. 449. 1014. 603. 200 mg. 432. All sequences have been deposited in GenBank under the accession numbers listed in Fig. 0. 830. IL. IL. budding cocci to rods Green colonies. 1 ml. / FEMS Microbiology Letters 218 (2003) 359^364 sorbs strongly near 800 and 850 nm) [16]. budding rods Light brown colonies. Microscopy was performed on an Olympus B-Max 60 photomicroscope. Germany Campus Lake Carbondale. 3. IL. 833. Monticello. USA Allerton Pond. thermophile In vivo Abs. higher dilutions did not yield positive enrichments over 6 weeks of incubation) . budding rods Dark green colonies.75 g. 830. 483. 604. 452. IL.2 g. The ¢nal pH was adjusted to 7 and the medium sterilized by autoclaving. 605. 1016. 452. USA Allerton Pond. Results 3. 397 425. In addition to pigmentation. 0. were low. 102 per ml or fewer. Carbondale. 482. 401 425. 832. 483. Ramsey. exported into PAUP [19]. trace elements [17]. 1015. 1015. 603. 428 423. budding rods. 0. USA Campus Lake. Enrichment. typical of Origin Freiburg. CaCl2 W2H2 O. 482. IL. ud.J. pigments. Urbana. 1015. budding rods Green colonies. The phylogeny of newly isolated Bchl b-containing phototrophs was determined by 16S ribosomal RNA gene sequencing. Ramsey. NH4 Cl. 0. 1016. 483. sodium lactate. All strains showed budding cell division. 604. inoculated tubes were incubated in a light tight plastic tray under the ¢lter (32‡C). USA Ramsey Lake. USA Ramsey Lake. Monticello.5 g. 604. and a phylogenetic distance tree generated using the Jukes^Cantor correction and a heuristic search pattern.3 g. 452. IL. green. 840. morphology. 404 402 401 400 401 Numbers in parentheses indicate the dilution of the original inoculum in which liquid enrichments yielded a positive culture (that is. 1015. B. These color di¡erences formed the basis for strain designations (G. 483. 424. 483. the highest dilution that yielded positive cultures was only 1032 . Sequencing methods were basically as previTable 1 Strains of B.360 G. 428 423. 483. However. 604. 1015.

cells were suspended in 30% bovine serum albumin. valerate (5 mM. +++). not determined. Absorption spectra of intact cells of B. 450 and 425 nm. fumarate. Other morphologies. However. 151^250 p. propanol (10 mM.u. supported good growth of all newly isolated strains but not of the type strain (Table 2).+). cells of brown or brown^green strains were somewhat larger and more irregularly rod-shaped (Table 1). A variety of alcohols and short chain fatty and organic acids supported photoheterotrophic growth of the new isolates. 3.d. / FEMS Microbiology Letters 218 (2003) 359^364 361 near 480. viridisa. G11. G3. fructose.7]. was equivalent to approximately 0. However.d. For strain DSM133T . the vast majority of green and brown-colored strains photocatabolized sugars.u. ++). ++). in all cases. +++. The latter peaks indicated that all strains contained the carotenoid neurosporene. for example. although cells of green-colored strains were typically small and coccus to egg-shaped.. Particularly good growth was obtained on malate. b The following substrates supported growth of each strain to approximately the same extent. and absorption properties of the new Bchl b-containing isolates is shown in Table 1. a number of substrates supported growth of the new isolates that were not used by the type strain of B.6]. Strains UN.d. Carbon nutrition In tests of carbon nutrition it was readily apparent that the new Bchl b-containing isolates were nutritionally versatile. . Three previously characterized strains of B. ++). +.J. like those of the type strain. ++.2. subtle di¡erences in carotenoid absorption maxima and the ratio of these maxima were observed in distinctly di¡erent colored strains (Fig. acetate or butyrate (10 mM. caproate (5 mM. and B9 only. +).u. Lactate (20 mM) 3 + + ++ +++ ++ ++ +++ ++ ++ + +++ + +++ +++ n. viridis [3. Blastochloris species [6. ++). Hoogewerf et al. n. cell morphology. their in vivo absorption spectra were quite similar (Table 1 and Fig. characteristic of B. +). Mannitol (10 mM) 3 3 + ++ ++ ++ ++ ++ ++ +++ 3 ++ ++ ++ ++ n. Growth was scored after 10 days as follows: 3. Surprisingly. viridis strain DSM 133T and Bchl b-containing strain B5. butanol (10 mM.u.G. 0^50 photometer units (p. A summary of the source. and in the carotenoid region Table 2 Carbon nutrition of new and established strains of B. 1. Ribose (10 mM) 3 3 3 ++ + + ++ 3 + 3 + ++ 3 + + n. DSM 133T [6].u. Lactose (10 mM) 3 3 3 ++ ++ ++ +++ +++ + +++ 3 + 3 +++ ++ n.. or K-ketoglutarate (20 mM. such as non-budding rods or spirilla. due to Bchl b. were not observed in cultures of the new isolates. Strains G15 and B9 grew weakly (+) on citrate. Negative controls lacking a substrate were less than 50 p. while one-carbon substrates (methanol. sucrose. Aspartate (20 mM) supported weak growth (+) of strains G3.d. including glucose. +). Methanol (10 mM) and formate (20 mM) did not support growth of any strain. formate) were not used by any strain (Table 2). glutamate (20 mM. malate or succinate (20 mM. Absorption maxima were obtained between 1012 and 1016 nm. Propionate and lactate. 100 p. however. Although none of the sugars tested supported growth of the type strain. ++). lactose and ribose.b Strain DSM133T UN G2 G3 G5 G6 G7 G8 G10 G11 G12 B4 B5 B7 B9 GI a Glucose (10 mM) 3 3 3 ++ ++ ++ ++ + + +++ 3 + + ++ ++ + Fructose (10 mM) 3 3 3 ++ ++ ++ ++ ++ + ++ 3 3 3 + ++ ++ Sucrose (10 mM) 3 3 3 ++ ++ ++ +++ ++ + ++ ++ ++ 3 + ++ n. ethanol (10 mM. and G11 grew weakly (+) on benzoate (5 mM)..2 mg bacterial dry weight ml31 of culture.d.) . viridis.d. sucrose and lactose Fig. Even more surprising were the results on sugars. Propionate (10 mM) 3 + ++ ++ + ++ + ++ ++ + + + ++ ++ + n.d. 1). 251^350 p. 51^150 p. Despite visible di¡erences in color among strains. Phototrophic growth in all cases in medium Enrich 1 containing the substrate indicated as sole carbon source. 1). For recording spectra. pyruvate.. pentanol (5 mM. viridis including the type strain were also tested in this connection and the results are summarized in Table 2.u.

The reason for the latter discrepancy is unclear. 2). 2). or were unable to compete with B. with the exception of the brown strain B9 (Fig. only detailed analyses of the carotenoid content of these strains could resolve this question. viridis isolates. only strain G2 showed the same negative pattern on all sugars as did strain DSM 133T (Table 2). still cluster tightly within the Blastochloris clade [22]. varying by at most. Hoogewerf et al. A major surprise emerging from this study was how the carbon nutritional properties of the new isolates were so distinct from that of the type strain. Rhodopseudomonas acidophila (Rhodoblastus acidophilus). 4. Our results certainly do not preclude the existence of other genera or species of Bchl b-containing anoxygenic phototrophs. viridis-type organisms under our enrichment conditions. viridis type strain (Fig. viridis but not by the type strain (Table 2). The sugar alcohol mannitol also supported good growth of most new strains but not of the type strain (Table 2). However. Phylogenetic distance tree of Bchl b-containing purple nonsulfur bacteria and closely related phototrophic species containing Bchl a. the results suggest that the diversity of these phototrophs is indeed quite limited. they were either absent in the habitats we sampled. Interestingly. In addition. and also showed strains B9 and GI to be distinct from the main clade of B. . The sequence of strain DSM133T generated herein was identical to that of the published sequence. Discussion The major objective of this study was to test the hypothesis that hidden diversity existed among culturable Bchl b-containing purple nonsulfur bacteria from freshwater habitats. 2). the 16S rRNA gene sequences of the new strains were nearly identical to that of the type strain. Only three newly isolated strains showed a similar pattern concerning growth on sugars as did strain DSM 133T (Table 2). The 16S rRNA gene of strain DSM 133T previously had been sequenced [2] but was sequenced here as an internal control on our methods.23]. However. ¢ve base substitutions over the approximately 1400 bases analyzed for each isolate (Fig. However.J. a moderately thermophilic hot spring isolate [21] that di¡ered from both B. and Rhodobacter capsulatus contain Bchl a. Color variation among strains of B.5% identical to the type strain. cultures were also grown to approximately the same densities (late exponential phase) in each case. 1) suggest that pigment di¡erences may indeed exist between these strains. sulfoviridis and B.7. 3. but in the present work sub- Fig. further work on the carotenoid composition of di¡erent colored B. our data. GenBank accession numbers are listed in parentheses following each strain designation. the aromatic compound benzoate. are strains of the species B. viridis has been previously observed [3] but the basis for this is unknown. In fact. A more distant relative was strain GI. Therefore. viridis. since for spectral analyses care was taken to grow all strains at the same light intensity and in the same medium . was used by a few of the new strains of B. 2). as regards sugar utilization in B. Slight di¡erences in absorption maxima and clear di¡erences in the ratios of spectral components in olive green versus brown strains (Fig. The di¡erences in absorption properties that we observed are unlikely to be due to growth conditions. But if such species exist. the latter was still 99. viridis strains could be enlightening.3. whose photocatabolism is restricted to only a few purple nonsulfur bacteria [20]. both brown and green. coupled with the fact that even metabolically unusual Bchl b-containing purple nonsulfur bacteria. thus con¢rming the previous sequence and indicating that our sequencing error rate was very low. Phylogeny The phylogeny of the new isolates was determined by 16S rRNA gene sequencing. However. / FEMS Microbiology Letters 218 (2003) 359^364 were particularly well used (Table 2). 2. Phylogenetic analysis using evolutionary distance showed the new isolates to group tightly with the B. For example. viridis. unable to grow in the media employed. however. Phylogenetic analysis using parsimony (data not shown) showed the same branching order and tight grouping of new strains as did the distance analyses. Green and brown strains were phylogenetically indistinguishable from the type strain. viridis by about 2% in 16S rRNA gene sequence (Fig. Rhodospirillum rubrum. the pattern displayed by the type strain (DSM 133T ) [7] (Table 2) is clearly the exception rather than the rule.362 G. It thus appears that the new isolates. our results that showed growth of the type strain on C4 ^C6 fatty acids are contrary to published reports [4. suggests that phylogenetic diversity is not a hallmark of this group. perhaps just to the species known at present. such as those capable of photocatabolizing toluene and crude oil.

N. Kompantseva. .E. and Madigan.. or other morphotypes that contain Bchl b exist in freshwater habitats.. A. Bacteriol. O. 73^78. capacities previously unrecognized in this species [7. C. strain GI [21]. Chlorobium tepidum. C. [3] Biebl. and Tru «per. [20] Gibson. 324^334. nov. [17] Wahlund. Mikrobiol.. Baltimore. [10] Madigan. N. 228^234. H. M. spirilla. H. (1989) Purple Nonsulfur Bacteria.A.. Bacteriol. nov.F.M. (1989) Genus Rhodopseudomonas... 107^112.A. 53. viridis expands dramatically beyond that listed for this species in Bergey’s Manual [7] and elsewhere [23]. [6] Whittenbury. pp. (1995) Taxonomy and physiology of phototrophic purple bacteria and green sulfur bacteria.. 267^273. and Imho¡. Zentralbl. The results of this study are the ¢rst experimental support of the current picture of biodiversity among purple nonsulfur bacteria containing Bchl b. A. 59. and Holt. G.I. 217^219. Bakteriol. for example.G.J. 1658^1661.A. gen. « Springer-Verlag. 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Gorlenko. sulfoviridis. Nickrent for help with DNA sequencing and analysis.). and Tru «per. Gorlenko. Achenbach. Bacteriol. viridis-photosynthetic budding bacteria.G. and McLee. Arch.. the mildly thermophilic Blastochloris sp. and one brown-colored isolate. Bacteriol. obligat phototrophes Bakterium. Parasiten. 73.G. Kompantseva.. In: The Prokaryotes (Starr. Steensland. Indeed. H. and Harwood.. viridis in nature.7]. 157. and Pfennig. M.F. establishment of a new taxon for this isolate may be warranted but will require further characterization. an alkaliphilic rod-to-coiled-shaped phototrophic heliobacterium from a Siberian soda lake. Syst. [7] Imho¡. 193^194. G. Arch.M.23]. 167^174. 156.. 50... A possible approach for extending our work would be to inspect the rRNA gene sequences generated here for signature sequences characteristic of this group and which are absent from all known Bchl a-containing species.G.M.).F. K.E. H. sulfoviridis.G. K. viridis was previously recognized [2]. H. and Gorlenko. where freshwater habitats support a phylogenetically broad species diversity [1. If such organisms do not exist. Microbiol. T. J. and Truper. The only exceptions were B.S. (1981) Ectothiorhodospira abdelmalekii sp. (1991) A thermophilic green sulfur bacterium from New Zealand hot springs.S. strain B9. (1999) Heliorestis daurensis. Sinauer. viridis on sugars and medium-chain-length fatty acids. viridis DSM 133T .. J.G. and Socolofsky. nov. As regards strain GI. Cox. Mikrobiologia 44. (1967) Rhodopseudomonas palustris and Rh. 81^91. (1967) A Thiococcus sp. (1981) Isolation of members of the family Rhodospirillaceae. nov. pp. then the diversity of Bchl b-containing phototrophs contrasts sharply with that of Bchl a-containing species. Hales. M. gen. R. 115^121.. M. Sunderland. (1975) A new species of purple budding bacteria containing bacteriochlorophyll b. viridis and B. Arch. K. J.. Bakteriol. and Traetteberg. [15] Bryantseva. pp. [8] Keppen.). and Schlegel.R.. Mikrobiol. (1995) Degradation of aromatic com- Acknowledgements This research was supported in part by a grant from the Illinois Council on Food and Agricultural Research (CFAR) Competitive Grants Program. Balows. MD. 1672^1677. sp. M.A. J. Hoogewerf et al. comparative sequencing supported the phenotypic studies and showed the majority of the new isolates to cluster tightly with B. Eds. spec. New York. J. Fluorescent labeling of only budding morphotypes in such studies would con¢rm the enrichment and isolation results reported here.. However.T.G. suggests that these may be important substrates for B. Arch. 114. S. Baltimore. Microbiol. Microbiol. J. Arch. [13] Eimhjellen. A. P. 155. and Madigan. nov. (2000) Thioalkalicococcus limnaeus gen..P. H. Eds. one could integrate them with FISH technology to examine natural samples or enrichment cultures. Eds.. M. Mikrobiol. Arch.I. 255^262. Syst. Abt.J. [11] Imho¡...F. In: Anoxygenic Photosynthetic Bacteria (Blankenship. pp. Madigan. Williams and Wilkins.T. J. and strengthen even further the contention that Bchl b-containing purple nonsulfur bacteria inhabiting freshwaters lack signi¢cant species diversity. Kluwer Academic Publishers. [16] Biebl. MD. and Holt J.. Eds.F.T. 1^15. J.F. and Giesbrecht.L (2000) PAUP*. M. a major lesson to be learned here is that physiological conclusions based on the results obtained from a single isolate can be quite misleading. Castenholz. and Imho¡.P. and Drews. Arch. (1977) Ectothiorhodospira halochloris sp. L. (1970) Thiocapsa pfennigii sp. E.T. 2157^2163.E. 47. nov. a new alkaliphilic purple sulfur bacterium with bacteriochlorophyll b. they have escaped our detection. I. H. B. in particular DNA:DNA hybridization. M. Truper. J. Dordrecht. 82^92. We thank Laurie A.W. References [1] Imho¡. its pigments and internal membrane system. In: « Bergey’s Manual of Systematic Bacteriology (Staley.).G.. a new species of the phototrophic sulfur bacteria. Stolp. Infektionskr Hyg. Intl. 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. and Madigan.F.. (1999) [22] Zengler. 65. Kluwer Academic Publishers. 204^ 212.364 G.T. In: The Prokaryotes.E. Eds. 991^1003. In: Anoxygenic Photosynthetic Bacteria (Blankenship. R. Heider. K. New York. Microbiol.G. F.. Madigan. 172. / FEMS Microbiology Letters 218 (2003) 359^364 Phototrophic utilization of toluene under anoxic conditions by a new strain of Blastochloris sulfoviridis. pp. J. (1989) Isolation and characterization of a mildly thermophilic nonsulfur purple bacterium containing bacteriochlorophyll b. R.).M. Dworkin. A.-H. M. Arch. pounds by nonsulfur purple bacteria. Dordrecht. ¤-Mora. and Widdel.. Truper.. Harder.. Hoogewerf et al. Rossello . Truper. and Bauer.). M. M. (Balows. S.. C.. (1992) The genus Rhodospirillum and « related genera. and Schleifer. K. [21] Resnick. J. 2nd ed. [23] Imho¡.G..J. Springer-Verlag. « H. pp. 2141^2155.. W.T. Lett. Eds. 165^170. FEMS Microbiol.E. H.

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