A Novel Organotrophic Nitrate-reducing Fe(II)-oxidizing Bacterium. Isolated from a Paddy Soil and Draft Genome Sequencing
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1 Electronic Supplementary Material (ESI) for RSC Advances. This journal is The Royal Society of Chemistry 2017 Supplementary information for A Novel Organotrophic Nitrate-reducing Fe(II)-oxidizing Bacterium Isolated from a Paddy Soil and Draft Genome Sequencing Indicates its Metabolic Versatility Min Hu 1, Pengcheng Chen 1,2,3,Weimin Sun 4, Fangbai Li 1*, Jianghu Cui 1 1 Guangdong Key Laboratory of Integrated Agro-environmental Pollution Control and Management, Guangdong Institute of Eco-Environmental Science & Technology, Guangzhou , P. R. China 2 Guangzhou Institute of Geochemistry, Chinese Academy of Sciences, Guangzhou , P. R. China 3 Graduate University of the Chinese Academy of Sciences, Beijing , P. R. China. 4 Department of Biochemistry and Microbiology, Rutgers University,New Brunswick 08901, NJ, USA These authors contributed equally to this work. * Corresponding author. Tel.: ; Fax: address: cefbli@soil.gd.cn. Running title: Nitrate-reducing Fe(II)-oxidizer from paddy soil 1
2 Table S1. Genes involved in ferrous iron oxidation of different physiological groups of the Fe(II) oxidizers. Species Physiology Genes Reference Acidithiobacillus ferrooxidans Acidophilic Cyc2, RusA, Cyc1, CycA1 1 Leptospirillum ferrooxidans Acidophilic Cyt572,Cyt579, Cytc 2 Sideroxydans lithotrophicus Micrro-aerobic MtoB, MtoA, CymA 3 Rhodopseudomonas palustris Phototrophic PioB, PioA, PioC 4 Rhodobacter ferrooxidans Phototrophic FoxE, FoxY 5 2
3 Table S2. Predicted cytochrome in Rhodocyclaceae sp. strain Paddy-1 from genome annotation. Gene AA No. gene Length length No. COG Pfam No. GO ORF_ NA PF00034 GO: , GO: , GO: ORF_ COG3258 PF00034 GO: , GO: , GO: ORF_ COG3245 PF00034 NA ORF_ COG2010 PF00034 NA ORF_ NA PF00034 GO: , GO: , GO: ORF_ COG2010 PF00034 GO: , GO: , GO: ORF_ COG4654 PF00034 GO: , GO: , GO: ORF_ COG4654 PF00034 GO: , GO: , GO: ORF_ COG2863 PF00034 GO: , GO: , GO: ORF_ COG3245 NA NA ORF_ COG3245 PF00034 GO: , GO: , GO: ORF_ NA PF00034 NA ORF_ COG4654 PF00034 NA ORF_ COG2863 PF00034 GO: , GO: , GO: ORF_ COG2863 PF00034 GO: , GO: , GO: ORF_ COG2010 PF00034 NA ORF_ COG2010 PF00034 GO: , GO: , GO: ORF_ COG4654 PF00034 GO: , GO: , GO: ORF_ COG2857 PF02167 GO: , GO: , GO: ORF_ COG1858 PF00034 GO: , GO: ORF_ COG2863 PF00034 GO: , GO: , GO: ORF_ COG3474 PF00034 GO: , GO: , GO: ORF_ COG2863 PF00034 GO: , GO: , GO: ORF_ NA PF01322 GO: , GO: , GO: ORF_ NA PF00034 GO: , GO: , GO: ORF_ COG2863 PF00034 GO: , GO: , GO: ORF_ COG3175 PF04442 GO: ORF_ COG3909 PF01322 GO: , GO: , GO: ORF_ COG2010 PF00034 NA ORF_ COG2010 NA NA ORF_ COG2010 PF00034 NA Description: COG1858: Cytochrome c peroxidase; COG2010: Cytochrome c, mono- and diheme variants; COG2857: Cytochrome c1; COG2863: Cytochrome c553; COG3175: Cytochrome oxidase assembly factor; COG3245: Cytochrome c5; COG3258: Cytochrome c, mono- and diheme variants; COG3474: Cytochrome c2; COG3909: Cytochrome c556; COG4235: Cytochrome c biogenesis factor; COG4654: Cytochrome c551/c552. PF00034: Cytochrome c; PF02167: Cytochrome C1 family; PF01322: Cytochrome C; PF04442: Cytochrome c 3
4 oxidase assembly protein CtaG/Cox11; PF07719: Tetratricopeptide repeat. GO : cytochrome-c oxidase activity; GO : iron ion binding; GO : copper ion binding; GO : electron carrier activity; GO : membrane; GO : oxidoreductase activity; GO : heme binding; GO : oxidation reduction. 4
5 Table S3. Predicted Fe ion homeostasis systems in Rhodocyclaceae sp. strain Paddy-1 from genomic annotation. (A) Ferredoxin Ferritin Gene Gene Length AA length No. COG No. Pfam No. GO ORF_ COG3411 PF01257 GO , GO , GO ORF_ COG0716 PF00258 NA ORF_ COG2146 NA GO , GO , GO ORF_ COG0348 PF11614 NA ORF_ COG0783 PF00210 GO , GO ORF_ COG0348 NA NA ORF_ COG0633 PF00111 GO , GO ORF_ COG0348 NA NA ORF_ COG3411 PF01257 GO , GO , GO ORF_ COG0348 PF11614 NA ORF_ COG1018 NA GO , GO ORF_ COG0633 PF00970 GO , GO ORF_ COG2146 PF00355 GO , GO , GO ORF_ COG0276 PF00762 GO , GO ORF_ COG1018 PF00970 GO , GO ORF_ COG1146 PF00037 NA ORF_ COG2193 PF00210 GO , GO ORF_ COG0633 PF00111 GO , GO ORF_ COG0348 NA NA (B) Transporters of ferrous and ferric ion Gene Gene AA No. No. No. Length length COG Pfam GO ORF_ NA PF02421 GO ,GO ORF_ COG1840 PF01547 GO ORF_ COG1178 PF00528 NA ORF_ COG1160 PF02421 GO , GO ORF_ COG2262 PF02421 GO ,GO ORF_ COG0672 FTR1 GO ,GO ORF_ COG0536 PF02421 GO ORF_ COG1840 PF01547 GO ,GO ORF_ COG1178 PF00528 NA ORF_ COG0614 PF01497 GO ,GO ORF_ COG1161 PF02421 NA ORF_ COG0735 PF01475 GO ,GO ORF_ COG0614 PF01497 GO ,GO
6 ORF_ COG4097 PF01794 GO ,GO ,GO ORF_ COG0486 PF02421 NA ORF_ COG0609 PF01032 GO ,GO ,GO ORF_ COG0012 PF02421 NA ORF_ COG0735 PF01475 GO ,GO ORF_ COG4097 PF01794 GO ,GO ,GO ORF_ COG2717 PF01794 GO ,GO ,GO ORF_ COG3064 PF02421 NA ORF_ COG3470 PF10634 NA Description: COG0012: Predicted GTPase, probable translation factor; COG0276: Protoheme ferro-lyase (ferrochelatase); COG0348: Polyferredoxin; COG0486: Predicted GTPases; COG0536: Predicted GTPases; COG0609: ABC-type Fe3+-siderophore transport system, permease component; COG0614: ABC-type Fe3+-hydroxamate transport system, periplasmic component; COG0633: Ferredoxin; COG0672: High-affinity Fe2+/Pb2+ permease; COG0716: Flavodoxins; COG0735: Fe 2+ /Zn 2+ uptake regulation proteins; COG0783: DNA-binding ferritin-like protein (oxidative damage protectant); COG1018: Flavodoxin reductases (ferredoxin-nadph reductases) family 1; COG1146: Ferredoxin; COG1160: Predicted GTPases; COG1161: Predicted GTPases; COG1178: ABC-type Fe3+ transport system, permease component; COG1840: ABC-type Fe3+ transport system, periplasmic component; COG2146: Ferredoxin subunits of nitrite reductase and ring-hydroxylating dioxygenases; COG2193: Bacterioferritin (cytochrome b1); COG2262: Predicted GTPases; COG2717: Predicted membrane protein; COG3064: Membrane protein involved in colicin uptake; COG3411: Ferredoxin; COG3470: Uncharacterized protein probably involved in high-affinity Fe2+ transport; COG4097: Predicted ferric reductase. PF00037: 4Fe-4S binding domain; PF00111: 2Fe-2S iron-sulfur cluster binding domain; PF00175: Oxidoreductase NAD-binding domain; PF00210: Ferritin-like domain; PF00258: Flavodoxin; PF00355: Rieske [2Fe-2S] domain; PF00528: Binding-protein-dependent transport system inner membrane component; PF00762: Ferrochelatase; PF00970: Oxidoreductase FAD-binding domain; PF01032: FecCD transport family; PF01257: Respiratory-chain NADH dehydrogenase 24 Kd subunit; PF01475: Ferric uptake regulator family; PF01497: Periplasmic binding protein; PF01547: Bacterial extracellular solute-binding protein; PF01794: Ferric reductase like transmembrane component; PF02421: Ferrous iron transport protein B; PF10634: Fe2+ transport protein; PF11614: Ubp3 associated protein Bre5. GO : transcription factor activity ; GO : ferrochelatase activity ; GO : transporter activity ; GO : iron ion transmembrane transporter activity ; GO : GTP binding ; GO : intracellular ; GO : regulation of transcription, DNA-dependent ; GO : heme biosynthetic process ; GO : transport ; GO : high-affinity iron ion transport ; GO : cellular iron ion homeostasis ; GO : ferric iron binding ; GO : electron carrier activity ; GO : membrane ; GO : integral to membrane ; GO : oxidoreductase activity ; GO : FAD binding ; GO : NAD or NADH binding ; GO : iron-sulfur cluster binding ; GO : 2 iron, 2 sulfur cluster binding ; GO : transmembrane transport ; GO : oxidation reduction. 6
7 Table S4. Predicted iron oxidase and related electron transfer system in Rhodocyclaceae sp. strain Paddy-1 by comparing to other oxidizing bacteria. gene Gene Length AA length Most related protein Similarity (E value) Score (Bits) No. COG No. Pfam No. GO ORF_ feob (S. oneidensis MR-1) 8.00E COG1160 PF02421 GO , GO ORF_ cyc1 (A. ferrooxidans 23270) 2.00E COG2863 PF00034 GO: , GO: , GO: ORF_ cyma (S. oneidensis MR-1) 7.00E COG3005 PF03264 NA ORF_ cyca-2 (A. ferrooxidans 23270) 2.00E COG2863 PF00034 GO: , GO: , GO: ORF_ cyc1 (A. ferrooxidans 23270) 9.00E COG2863 PF00034 GO: , GO: , GO: ORF_ feob (S.oneidensis MR-1) 1.00E COG0012 PF02421 NA ORF_ cyc1 (A. ferrooxidans 23270) 1.00E COG2863 PF00034 GO: , GO: , GO: ORF_ cyc2 (A. ferrooxidans 23270) 3.00E NA NA NA ORF_ cyca-1 (A. ferrooxidans 23270) 1.00E COG2863 PF00034 GO: , GO: , GO: ORF_ cyma (S.oneidensis MR-1) 1.00E COG3005 PF03264 NA Description COG0012: Predicted GTPase, probable translation factor; COG1160: Predicted GTPases; COG2863: Cytochrome c553; COG3005: Nitrate/TMAO reductases, membrane-bound tetraheme cytochrome c subunit. PF00034: Cytochrome c; PF02421: Ferrous iron transport protein B; PF03264: NapC/NirT cytochrome c family, N-terminal region. GO : iron ion binding ; GO : GTP binding ; GO : intracellular ; GO : electron carrier activity ; GO : heme binding. 7
8 Supplementary Figures Fig. S1 Transmission electron micrographs of a single cell of Rhodocyclaceae sp. strain Paddy-1 in the presence of 10 mm nitrate, 5 mm FeCl 2 and 5 mm acetate at day 12 of incubation time. 8
9 Fig. S2 Neighbor-joining tree based on 16S rrna sequences showing the phylogenetic affiliation of Rhodocyclaceae sp. strain Paddy-1 and evolutionary distance to other nitrate-reducing Fe(II)-oxidizing bacteria. Bootstrap values were determined on the basis of results of 1,000 replicates. Accession numbers are listed after the bacterium. The scale bar represents evolutionary distance as 0.02 change per nucleotide position. The numbers given are bootstrap values. Identified nitratedependent Fe(II)-oxidizing bacteria are shown in blue color of the font. 9
10 Fig. S3 Oxidation of dissolved Fe(II) in cultures of the nitrate-reducing Fe(II)- oxidizing Rhodocyclaceae sp. strain Paddy-1 using different organic carbon (5 mm) as an electron donor. The prestarved cell ( 10 9 cells ml 1 ) were cultured in the basal medium containing 5 mm Fe(II) and 10 mm of nitrate. Data were all presented as means ± standard deviations (SD) of triplicate. When not shown, error bars are smaller than the symbol size. 10
11 Fig. S4 X-ray diffraction (XRD) spectrum of the Rhodocyclaceae sp. strain Paddy-1 culture. No distinct diffractive acuti-apices implies the formation of amorphous iron oxides. 11
12 Fig. S5 Results of ANI calculations using JSpecies software of strain Paddy-1 with respect to the reported nitrate-reducing Fe(II)-oxidizing species. 12
13 Fig. S6 Eggnog categories of the genes predicted from nitrate-reducing Fe(II)- oxidizers. 13
14 Fig. S7 KEGG categories of the genes predicted from nitrate-reducing Fe(II)- oxidizers. 14
15 Fig. S8 Clustering of the nitrate-reducing Fe(II)-oxidizers based on functional annotation of the genes by eggnog database on the gene abundance. The color code indicates the relative abundance of the genes after z-score normalization. 15
16 Fig. S9 Clustering of the nitrate-reducing Fe(II)-oxidizers based on functional annotation of the genes by KEGG pathways on the gene abundance. The color code indicates the relative abundance of the genes after z-score normalization. 16
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