Hrm2, a marine sulfate reducer oxidizing organic carbon completely to carbon dioxide




НазваниеHrm2, a marine sulfate reducer oxidizing organic carbon completely to carbon dioxide
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Received: 09-Jul-2008

Accepted: 25-Oct-2008


Genome sequence of Desulfobacterium autotrophicum HRM2, a marine sulfate reducer oxidizing organic carbon completely to carbon dioxide


Axel W. Strittmatter,* Heiko Liesegang, Ralf Rabus,2,3§* Iwona Decker,1 Judith Amann,2 Sönke Andres,1 Anke Henne,1 Wolfgang Florian Fricke,1 Rosa Martinez-Arias,1 Daniela Bartels,4 Alexander Goesmann,4 Lutz Krause,4 Alfred Pühler,5 Hans-Peter Klenk,6 Michael Richter,2 Margarete Schüler,2 Frank Oliver Glöckner,2 Anke Meyerdierks,2 Gerhard Gottschalk,1 Rudolf Amann,2


§ these authors contributed equally to the work

* corresponding authors

E-mail astritt@gwdg.de; Tel. XXX; Fax XXX

E-mail rrabus@mpi-bremen.de; Tel. (+49) 798 3884; Fax (+49) 441 798 3404


1 Göttingen Genomics Laboratory, Georg-August-University, Grisebachstr. 8, D-37077 Göttingen, Germany.

2 Max Planck Institute for Marine Microbiology, Celsiusstr. 1, D-28359 Bremen, Germany.

3 Institute for Chemistry and Biology of the Marine Environment (ICBM), Carl von Ossietzky University Oldenburg, Carl-von-Ossietzky Str. 9-11, D-26111 Oldenburg, Germany.

4 Center for Biotechnology (CeBiTec), Bielefeld University, Universitätsstr. 37, D-33615 Bielefeld, Germany.

5 Lehrstuhl für Genetik, Fakultät für Biologie, Universität Bielefeld, D-33594 Bielefeld, Germany.

6 DSMZ - Deutsche Sammlung von Mikroorganismen und Zellkulturen GmbH, Inhoffenstraße 7 B, D-38124 Braunschweig, Germany.


present adresses: D.I., Landeskriminalamt Wiesbaden (LKA Wiesbaden), Hölderlinstr. 5, D-65187 Wiesbaden, Germany; A.S., Karolinska Institutet, SE-171 77 Stockholm, Sweden; A.H., QIAGEN GmbH, Qiagen Strasse 1, D-40724 Hilden, Germany; W. F. F., Institute for Genome Sciences (IGS), Department of Microbiology & Immunology, University of Maryland School of Medicine, 20 Penn Street, Baltimore MD 21201, United States of America; M.-A. R., Helmholtz Zentrum für Infektionsforschung, Abteilung Genomanalyse, Mascheroder Weg 1, D-38124 Braunschweig, Germany.


Re-use of this article is permitted in accordance with the Creative Commons Deed, Attribution 2.5, which does not permit commercial exploitation.

Summary

Sulfate-reducing bacteria belonging to the metabolically versatile Desulfobacteriaceae are abundant in marine sediments and contribute to the global carbon cycle by complete oxidation of organic compounds. Desulfobacterium autotrophicum HRM2 is the first member of this ecophysiologically important group with a now available genome sequence. With 5.6 megabasepairs (Mbp) the genome of Db. autotrophicum HRM2 is about two Mbp larger than the sequenced genomes of other sulfate reducers (SRB). A high number of genome plasticity elements (>100 transposon-related genes), several regions of GC-discontinuity and a high number of repetitive elements (132 paralogues genes Mbp-1) point to a different genome evolution when comparing with Desulfovibrio spp.. The metabolic versatility of Db. autotrophicum HRM2 is reflected in the presence of genes for the degradation of a variety of organic compounds including long chain fatty acids and for the Wood-Ljungdahl-pathway, which enables the organism to completely oxidize acetyl-CoA to CO2 but also to grow chemolithautotrophically. The presence of more than 250 proteins of the sensory-/regulatory-protein families should enable Db. autotrophicum HRM2 to efficiently adapt to changing environmental conditions. Genes encoding periplasmic or cytoplasmic hydrogenases and formate dehydrogenases have been detected as well as genes for the transmembrane TpII-c3-, Hme, and Rnf-complexes. Genes for subunits A, B, C, and D as well as for the proposed novel subunits L and F of the heterodisulfide reductases are present. This enzyme is involved in energy conservation in methanoarchaea and it is speculated that it exhibits a similar function in the process of dissimilatory sulfate reduction in Db. autotrophicum HRM2.

Introduction

Shelf sediments receive the highest input of organic carbon among marine systems. They are mostly anoxic and more than 50% of the mineralization of the organic carbon is coupled in these environments to bacterial sulfate reduction (Jørgensen, 1982; Canfield et al., 1993). Typically, sulfate-reducing bacteria (SRB) utilize small reduced molecules mostly fermentation products, e.g. acetate, lactate or ethanol, placing them together with syntrophs and methanogens at the end of the anaerobic food chain (Widdel, 1988; Rabus et al., 2000). The observed high mineralization rates coupled to bacterial sulfate reduction are indicative for complete oxidation of organic substrates to CO2 (Fenchel and Jørgensen, 1977; Jørgensen, 1982). While the frequently isolated and intensively studied Desulfovibrio spp. oxidize organic substrates only to the level of acetate, complete oxidation was first demonstrated for Desulfotomaculum acetoxidans (Widdel and Pfennig, 1977), Desulfobacter postgatei (Widdel and Pfennig, 1981) and Desulfobacterium autotrophicum HRM2 (Brysch et al., 1987). The nutritionally versatile Db. autotrophicum HRM2 oxidizes a variety of organic acids and alcohols to CO2 and, in addition, is able to grow chemolithoautotrophically with H2, CO2 and sulfate. While Desulfobacter spp. so far investigated employ modified citric acid cycles for terminal oxidation of acetyl-CoA (Brandis-Heep et al., 1983), the Wood-Ljungdahl pathway is used by Db. autotrophicum HRM2 (Schauder et al., 1986) with acetyl-CoA synthase/carbon monoxide dehydrogenase (ACS/CODH) as the key enzyme complex. This pathway presumably also functions in the reductive direction for CO2-fixation under autotrophic growth conditions (Länge et al., 1989; Schauder et al., 1989). Corroborating their ecophysiological role members of the Desulfobacteriaceae were repeatedly observed to dominate the population of sulfate-reducing bacteria in various anoxic habitats, while Desulfovibrio species were mostly absent (e.g. Teske et al., 1998; Llobet-Brossa et al., 2002; Dhillon et al., 2003). Recognition of the environmental significance of sulfate-reducing bacteria resulted in several genome-sequencing projects (for overview see Rabus and Strittmatter, 2007). Db. autotrophicum HRM2 is the first representative of the ecophysiologically important group of the completely oxidizing sulfate reducers. The genome sequence presented here reflects its high metabolic versatility and reveals novel insights into the bioenergetics of dissimilatory sulfate reduction.

Results and discussion


GENERAL GENOME FEATURES

Genome size and coding sequences. The genome of Db. autotrophicum HRM2 consists of two circular replicons, a chromosome of 5,589,073 base pairs (bp) encoding 4,871 CDS (accession number CP001087) and a plasmid (pHRM2a) of 62,962 bp encoding 76 CDS (CP001088). Three of these encode proteins for plasmid maintenance of the Par-family, the remaining CDS only share weak similarities with other proteins. Therefore, the plasmid does not carry any known physiological function. With 5.5 Mbp the chromosome of Db. autotrophicum HRM2 is about 2 Mbp larger than those of the other three -proteobacterial SRB with to date published genomes: Desulfotalea psychrophila LSv54 (Rabus et al., 2004), Desulfovibrio vulgaris Hildenborough (Heidelberg et al., 2004) and Dv. desulfuricans G20 (Copeland et al., 2005). The principal features of the Db. autotrophicum HRM2 genome in comparison to other sequenced sulfate- and sulfur-reducing prokaryotes are summarized in Table 1. A general overview is given in the supplemental Figure (Fig.) S1.


Paralogous proteins and repeats. The Db. autotrophicum HRM2 genome contains 2,357 exact DNA repeats greater than or equal to 50 bp, giving an average of 422 repeats per Mbp (Mbp-1). The total number of genes with one or more paralogues is 1,460. This corresponds to 265 genes with paralogues per Mbp, and is the highest number of repetitive DNA stretches and the highest number of paralogous genes in all compared genomes (Tables 1, S1 and S2). The distribution of the number of paralogous genes is strongly biased; e.g. key enzymes of the sulfate reduction pathway, CO2-fixation and central metabolism are unique or have only few copies ( 3). This is in clear contrast to genes for substrate utilization where for instance 11 paralogues of acyl-CoA synthetases and 17 paralogues of acyl-CoA dehydrogenases could be identified. The presence of multiple copies of metabolic genes could represent an ecological advantage allowing an expansion of functional capabilities in response to varying environmental conditions (e.g. redox states or substrate concentrations).


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