Extending the models for iron and sulfur oxidation in the extreme acidophile Acidithiobacillus ferrooxidans.
BACKGROUND
Acidithiobacillus ferrooxidans gains energy from the oxidation of ferrous iron and various reduced inorganic sulfur compounds at very acidic pH. Although an initial model for the electron pathways involved in iron oxidation has been developed, much less is known about the sulfur oxidation in this microorganism. In addition, what has been reported for both iron and sulfur oxidation has been derived from different A. ferrooxidans strains, some of which have not been phylogenetically characterized and some have been shown to be mixed cultures. It is necessary to provide models of iron and sulfur oxidation pathways within one strain of A. ferrooxidans in order to comprehend the full metabolic potential of the pangenome of the genus.


RESULTS
Bioinformatic-based metabolic reconstruction supported by microarray transcript profiling and quantitative RT-PCR analysis predicts the involvement of a number of novel genes involved in iron and sulfur oxidation in A. ferrooxidans ATCC23270. These include for iron oxidation: cup (copper oxidase-like), ctaABT (heme biogenesis and insertion), nuoI and nuoK (NADH complex subunits), sdrA1 (a NADH complex accessory protein) and atpB and atpE (ATP synthetase F0 subunits). The following new genes are predicted to be involved in reduced inorganic sulfur compounds oxidation: a gene cluster (rhd, tusA, dsrE, hdrC, hdrB, hdrA, orf2, hdrC, hdrB) encoding three sulfurtransferases and a heterodisulfide reductase complex, sat potentially encoding an ATP sulfurylase and sdrA2 (an accessory NADH complex subunit). Two different regulatory components are predicted to be involved in the regulation of alternate electron transfer pathways: 1) a gene cluster (ctaRUS) that contains a predicted iron responsive regulator of the Rrf2 family that is hypothesized to regulate cytochrome aa3 oxidase biogenesis and 2) a two component sensor-regulator of the RegB-RegA family that may respond to the redox state of the quinone pool.


CONCLUSIONS
Bioinformatic analysis coupled with gene transcript profiling extends our understanding of the iron and reduced inorganic sulfur compounds oxidation pathways in A. ferrooxidans and suggests mechanisms for their regulation. The models provide unified and coherent descriptions of these processes within the type strain, eliminating previous ambiguity caused by models built from analyses of multiple and divergent strains of this microorganism.
Quatrini
Raquel
R
Center for Bioinformatics and Genome Biology, MIFAB, Fundación Ciencia para la Vida and Depto. de Ciencias Biologicas, Universidad Andres Bello, Santiago, Chile. rquatrini@yahoo.com.ar
Appia-Ayme
Corinne
C
Denis
Yann
Y
Jedlicki
Eugenia
E
Holmes
David S
DS
Bonnefoy
Violaine
V
D042763:Acidithiobacillus / Q000235:genetics* / Q000378:metabolism; D019295:Computational Biology; D020869:Gene Expression Profiling; D005798:Genes, Bacterial; D016680:Genome, Bacterial; D007501:Iron / Q000378:metabolism*; D055432:Metabolomics; D020411:Oligonucleotide Array Sequence Analysis; D010084:Oxidation-Reduction; D012329:RNA, Bacterial / Q000235:genetics; D013457:Sulfur Compounds / Q000378:metabolism*
D012329:RNA, Bacterial; D013457:Sulfur Compounds; D007501:Iron
PLoS One. 2008 Jan 30;3(1):e1514
18231600
J Mol Biol. 2007 Jan 19;365(3):732-43
17095009
Appl Environ Microbiol. 1991 Jul;57(7):2057-62
16348525
J Mol Biol. 2006 Apr 21;358(1):132-44
16497328
Biochim Biophys Acta. 1982 Nov 30;683(2):89-117
6295474
Biochim Biophys Acta. 1998 Nov 26;1443(1-2):99-112
9838063
BMC Genomics. 2008 Dec 11;9:597
19077236
Nucleic Acids Res. 2001 Jan 1;29(1):123-5
11125067
J Biol Chem. 2008 Sep 19;283(38):25803-11
18632666
Biosci Biotechnol Biochem. 2007 Nov;71(11):2735-42
17986789
Biochim Biophys Acta. 2006 Dec;1757(12):1676-82
17046710
Appl Environ Microbiol. 1999 Nov;65(11):4781-7
10543786
Microbiology (Reading). 1997 Sep;143 ( Pt 9):2891-2902
9308173
Annu Rev Biochem. 2006;75:69-92
16756485
Microbiol Mol Biol Rev. 2004 Jun;68(2):263-79
15187184
Eur J Biochem. 1998 Apr 1;253(1):263-9
9578485
J Biol Chem. 2000 Mar 24;275(12):8283-6
10722656
Mol Microbiol. 2004 Aug;53(4):1147-60
15306018
Biochemistry. 2004 Jan 27;43(3):773-81
14730982
Eur J Biochem. 2004 Mar;271(6):1106-16
15009189
Appl Environ Microbiol. 1988 Jan;54(1):153-7
3345075
Nature. 2004 Mar 4;428(6978):37-43
14961025
Appl Environ Microbiol. 2008 Dec;74(24):7723-32
18931292
FEBS Lett. 2002 Feb 13;512(1-3):263-8
11852093
Biosci Biotechnol Biochem. 2004 Dec;68(12):2519-28
15618623
Eur J Biochem. 1999 Jul;263(1):79-84
10429190
Appl Environ Microbiol. 2002 Apr;68(4):1837-45
11916703
Adv Microb Physiol. 2009;54:103-200
18929068
Microbiol Mol Biol Rev. 1997 Sep;61(3):337-76
9293186
J Bacteriol. 2000 Jun;182(12):3602-6
10852897
Nat Genet. 2000 May;25(1):25-9
10802651
Appl Environ Microbiol. 1992 Nov;58(11):3767-9
16348814
Int J Syst Evol Microbiol. 2003 Jan;53(Pt 1):113-119
12656161
J Biol Chem. 1989 May 5;264(13):7129-34
2540175
ISME J. 2008 May;2(5):542-50
18463612
Appl Environ Microbiol. 2008 Nov;74(21):6808-10
18791023
Ann N Y Acad Sci. 1988;550:325-36
2854404
Adv Exp Med Biol. 2008;631:131-48
18792686
FEMS Microbiol Lett. 1998 Oct 15;167(2):171-7
9809418
J Bacteriol. 2002 Mar;184(5):1498-501
11844787
J Mol Biol. 2008 Dec 31;384(5):1287-300
18952098
FEMS Microbiol Lett. 2007 May;270(1):58-66
17302937
Genome Res. 2005 Jul;15(7):1015-22
15998914
Biochim Biophys Acta. 2007 May;1767(5):393-400
17448440
J Proteome Res. 2005 Jan-Feb;4(1):63-70
15707358
J Bacteriol. 2002 Jan;184(1):313-7
11741873
Appl Environ Microbiol. 2007 Apr;73(8):2491-7
17322327
Microbiology (Reading). 2005 Dec;151(Pt 12):4127-4137
16339958
Can J Microbiol. 2001 May;47(5):424-30
11400733
EMBO J. 1997 Feb 17;16(4):739-49
9049303
J Biol Chem. 1981 Nov 25;256(22):11905-10
6271763
OMICS. 2005 Spring;9(1):13-29
15805776
Curr Opin Microbiol. 2005 Jun;8(3):253-9
15939347
Biochemistry. 2007 Nov 6;46(44):12875-85
17929940
Curr Opin Microbiol. 2003 Apr;6(2):181-5
12732309
Proteomics. 2006 Aug;6(15):4278-85
16807941
Microbiology (Reading). 2007 Oct;153(Pt 10):3478-3498
17906146
Appl Environ Microbiol. 2008 Feb;74(3):682-92
18083856
Biochem J. 2004 Jul 1;381(Pt 1):137-46
15030315
Appl Environ Microbiol. 2004 Aug;70(8):4491-8
15294777
Prep Biochem Biotechnol. 2007;37(2):101-11
17454821
J Bacteriol. 1992 Jun;174(12):4189-92
1597434
Can J Biochem. 1968 May;46(5):457-61
4968764
Biochim Biophys Acta. 2002 Sep 10;1555(1-3):37-43
12206888
Mol Cell. 2006 Jan 6;21(1):97-108
16387657
Arch Biochem Biophys. 2002 Oct 15;406(2):275-88
12361716
Microbiology (Reading). 2007 Jan;153(Pt 1):102-10
17185539
J Biotechnol. 2007 Oct 15;132(1):16-22
17904676
FEMS Microbiol Lett. 2001 Sep 11;203(1):1-9
11557133
J Biochem Mol Biol. 2006 Mar 31;39(2):178-82
16584633
Chem Biol Interact. 2003 Feb 1;143-144:271-8
12604213
Microbiology (Reading). 2003 Jul;149(Pt 7):1699-1710
12855721
Appl Environ Microbiol. 2008 Jul;74(14):4454-62
18469132
J Biol Chem. 2001 Sep 7;276(36):33588-95
11443125
Biochim Biophys Acta. 2004 Jun 7;1656(2-3):114-26
15178473
Adv Microb Physiol. 1998;39:235-89
9328649
Biometals. 2007 Jun;20(3-4):333-45
17387580
Biol Chem. 2005 Oct;386(10):961-70
16218868
Biochemistry. 2005 Jul 12;44(27):9545-54
15996109
Microbiology (Reading). 2004 Jul;150(Pt 7):2113-2123
15256554
Microbiology (Reading). 2009 Apr;155(Pt 4):1302-1309
19332831
Nucleic Acids Res. 2009 Jan;37(Database issue):D412-6
18940858
Can J Biochem. 1971 Oct;49(10):1125-30
5142118