High genetic and physiological diversity of sulfate-reducing bacteria isolated from an oligotrophic lake sediment

Sass, Henrik; Wieringa, Elze B. A.; Cypionka, Heribert; Babenzien, Hans‐Dietrich; Overmann, Jörg

doi:10.1007/s002030050639

Cited by 73 publications

(52 citation statements)

References 38 publications

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“…Nine different ERIC-PCR fingerprint patterns were detected among the 11 strains, revealing the highest genetic diversity within one 16S rRNA phylotype known so far. In previous studies, a maximum of three different genotypes with identical 16S rRNA gene sequences were recovered from one environment (27,48).…”

Section: Resultsmentioning

confidence: 99%

“…Nevertheless, some of the 16S rRNA gene sequences (e.g., the two rrsE genes) are identical in the two organisms. Similarly, genomic fingerprinting (48,50,57) and analysis of fosmid libraries of DNA fragments from marine samples (6) have indicated that nonpathogenic bacteria with identical 16S rRNA gene sequences but distinctly different genomes coexist in natural ecosystems (46). The term microdiversity has been used to describe the phenomenon of phylogenetically closely related but physiologically distinct bacterial populations (32).…”

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confidence: 99%

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Ecological Significance of Microdiversity: Identical 16S rRNA Gene Sequences Can Be Found in Bacteria with Highly Divergent Genomes and Ecophysiologies

Jaspers

Overmann

2004

Appl Environ Microbiol

305

251

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A combination of cultivation-based methods with a molecular biological approach was used to investigate whether planktonic bacteria with identical 16S rRNA gene sequences can represent distinct eco-and genotypes. A set of 11 strains of Brevundimonas alba were isolated from a bacterial freshwater community by conventional plating or by using a liquid most-probable-number (MPN) dilution series. These strains had identical 16S rRNA gene sequences and represented the dominant phylotype in the plateable fraction, as well as in the highest positive dilutions of the MPN series. However, internally transcribed spacer and enterobacterial repetitive intergenic consensus PCR fingerprinting analyses, as well as DNA-DNA hybridization analyses, revealed great genetic diversity among the 11 strains. Each strain utilized a specific combination of 59 carbon substrates, and the niche overlap indices were low, suggesting that each strain occupied a different ecological niche. In dialysis cultures incubated in situ, each strain had a different growth rate and cell yield. We thus demonstrated that the B. alba strains represent distinct populations with genetically determined adaptations and probably occupy different ecological niches. Our results have implications for assessment of the diversity and biogeography of bacteria and increase the perception of natural diversity beyond the level of 16S rRNA gene sequences.Analysis of 16S rRNA gene sequences has become the primary approach for studying the natural occurrence and distribution of bacteria in a culture-independent manner (3). The vertical and seasonal distributions of distinct 16S rRNA gene sequences (phylotypes) within one ecosystem have been used to infer the ecological niches of bacteria (40,56). This approach is especially valuable if the physiology of bacteria that have not been cultured yet is to be elucidated.In many cases phylogenetically closely related bacteria (whose 16S rRNA sequences differ by between 2.7 and 0.3%) have been detected in the same freshwater, marine, or soil habitat (19,32,43,56). According to macroecological principles of competitive exclusion, physiologically similar microorganisms should not co-occur in nutrient-poor systems which are dominated by physical and chemical fluctuations (40). Accordingly, phylogenetically closely related bacteria coexisting in the same habitat occupy distinct ecological niches (19,32,43,56).For pathogenic bacteria it is well established that even phylogenetically identical strains or species can exhibit distinct ecophysiological properties. Certain serovars of Mycobacterium intracellulare (10), serovars of Ochrobactrum anthropi (27), strains of Yersinia pestis and Yersinia pseudotuberculosis (55), or strains of Bacillus anthracis and Bacillus cereus (4) contain identical 16S rRNA gene sequences. These phylogenetically identical organisms are also genetically highly similar based on DNA-DNA hybridization data (Table 1) but clearly represent different ecotypes based on their virulence properties or host ranges. Often, p...

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Section: Resultsmentioning

confidence: 99%

mentioning

confidence: 99%

Ecological Significance of Microdiversity: Identical 16S rRNA Gene Sequences Can Be Found in Bacteria with Highly Divergent Genomes and Ecophysiologies

Jaspers

Overmann

2004

Appl Environ Microbiol

305

251

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“…DNA and RNA of each sediment horizon were extracted from 1.5 ml wet sediment by bead-beating, phenol extraction and isopropanol precipitation as described previously (Sahm & Berninger 1998). PCR amplification specific for SRB of the δ-subclass of Proteobacteria was carried out with the forward primer SRB385 carrying a GC-clamp and the reverse primer 907 (Sass et al 1998). DGGE, excision of bands, reamplification, and sequencing were performed as previously described (Muyzer et al 1996).…”

Section: Somentioning

confidence: 99%

“…This might be due to the activity of sulfate reducers at this site, which have so far not been used in experiments on isotope discrimination. In addition, it is known that H 2 S is, to a significant portion, reoxidized, so that sulfur species with intermediate oxidation states may be formed (Jørgensen 1982b), and such that bacterial disproportionation of the latter may lead to the formation of 32 S-enriched H 2 S (Canfield et al 1998, Cypionka et al 1998, Böttcher et al 2001. Indeed, bacteria which are able to disproportionate elemental sulfur, for instance, have been enriched from the sediments at Site Dangast and shown experimentally to discriminate sulfur isotopes (Canfield et al 1998).…”

Section: Biogeochemistry Of the Sedimentmentioning

confidence: 99%

Community structure and activity of sulfate-reducing bacteria in an intertidal surface sediment: a multi-method approach

Llobet-Brossa

Rabus

Böttcher

et al. 2002

Aquat. Microb. Ecol.

109

111

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The community structure of sulfate-reducing bacteria (SRB) in an intertidal mud flat of the German Wadden Sea (Site Dangast, Jade Bay) was studied and related to sedimentary biogeochemical gradients and processes. Below the penetration depths of oxygen (~3 mm) and nitrate (~4 mm), the presence of dissolved iron and manganese and the absence of dissolved sulfide indicated suboxic conditions within the top 10 cm of the sediment. Moderate to high bacterial sulfate reduction rates were measured with radiotracers throughout the sediment, and dissimilatory sulfate reduction was also demonstrated by the presence of acid-volatile sulfides (AVS, essentially iron monosulfide). Stable sulfur isotope discrimination between dissolved sulfate and AVS was dominated by sulfate reduction. The diversity of SRB was studied using denaturant gradient gel electrophoresis of 16S rDNA, phospholipid fatty acid analysis and counting viable cells with the most probable number technique. Phylogenetic groups of SRB identified with these techniques were almost evenly distributed throughout the top 20 cm of the sediment. Application of fluorescence in situ hybridization, however, demonstrated a maximum of active members of the Desulfovibrio and Desulfosarcina-Desulfococcus-Desulfofrigus groups between 2 and 3 cm depth. These 2 groups encompass acetate and lactate utilizing SRB. The coincidence of this SRB maximum with a local maximum of sulfate reduction rates and the depletion of acetate and lactate reflects the microbiological processes related to sulfate reduction.

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“…However, such "microdiversity" has been reported to make up a significant fraction of the sequence composition of clone libraries (4,10,13,24). That it potentially signifies functional differences is suggested by comparisons between closely related 16S rRNA sequences and physiological properties of isolates (12,32,36) or overall genome architectures (2,18,31,35). In addition, reports of relatively large divergence among rRNA genes between operons have suggested that HGT may affect rRNA genes to a larger extent than was previously assumed (28,40,41,43).…”

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Divergence and Redundancy of 16S rRNA Sequences in Genomes with Multiple rrn Operons

et al. 2004

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The level of sequence heterogeneity among rrn operons within genomes determines the accuracy of diversity estimation by 16S rRNA-based methods. Furthermore, the occurrence of widespread horizontal gene transfer (HGT) between distantly related rrn operons casts doubt on reconstructions of phylogenetic relationships. For this study, patterns of distribution of rrn copy numbers, interoperonic divergence, and redundancy of 16S rRNA sequences were evaluated. Bacterial genomes display up to 15 operons and operon numbers up to 7 are commonly found, but ϳ40% of the organisms analyzed have either one or two operons. Among the Archaea, a single operon appears to dominate and the highest number of operons is five. About 40% of sequences among 380 operons in 76 bacterial genomes with multiple operons were identical to at least one other 16S rRNA sequence in the same genome, and in 38% of the genomes all 16S rRNAs were invariant. For Archaea, the number of identical operons was only 25%, but only five genomes with 21 operons are currently available. These considerations suggest an upper bound of roughly threefold overestimation of bacterial diversity resulting from cloning and sequencing of 16S rRNA genes from the environment; however, the inclusion of genomes with a single rrn operon may lower this correction factor to ϳ2.5. Divergence among operons appears to be small overall for both Bacteria and Archaea, with the vast majority of 16S rRNA sequences showing <1% nucleotide differences. Only five genomes with operons with a higher level of nucleotide divergence were detected, and Thermoanaerobacter tengcongensis exhibited the highest level of divergence (11.6%) noted to date. Overall, four of the five extreme cases of operon differences occurred among thermophilic bacteria, suggesting a much higher incidence of HGT in these bacteria than in other groups.

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High genetic and physiological diversity of sulfate-reducing bacteria isolated from an oligotrophic lake sediment

Cited by 73 publications

References 38 publications

Ecological Significance of Microdiversity: Identical 16S rRNA Gene Sequences Can Be Found in Bacteria with Highly Divergent Genomes and Ecophysiologies

Ecological Significance of Microdiversity: Identical 16S rRNA Gene Sequences Can Be Found in Bacteria with Highly Divergent Genomes and Ecophysiologies

Community structure and activity of sulfate-reducing bacteria in an intertidal surface sediment: a multi-method approach

Divergence and Redundancy of 16S rRNA Sequences in Genomes with Multiple rrn Operons

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