Table 2.
List of the top 66 significantly differentially expressed proteins in B. diazoefficiens cells grown under microoxic conditions (0.5% O2) in comparison to oxic conditions (62 proteins upregulated that constitute the “core microoxic proteome,” and four proteins downregulated; multiple testing corrected p-value ≤ 0.2).
| Locus_taga | Productb | Gene namec | Queryd | log2 FC (microoxic vs. oxic)e | FC (microoxic vs. oxic)f | FC (soybean bacteroids vs. oxic)g | NifA+RpoN1 targetsh | FixK2 targetsi |
|---|---|---|---|---|---|---|---|---|
| Sixty-two proteins showing increased expression in microoxic conditions in comparison to oxic conditions (p-value ≤ 0.2) | ||||||||
| Bdiaspc4_00855 | Aminocyclopropane-1-carboxylate deaminase/D-cysteine desulfhydrase family protein | acdS | blr0241 | 2.8 | 4.8 | 20.1 | – | – |
| Bdiaspc4_05275 | Benzoyl-CoA-dihydrodiol lyase | – | blr1080 | 3.1 | – | 25.4 | – | – |
| Bdiaspc4_06495 | Propionyl-CoA synthetase | acs | blr1309 | 1.6 | 3.1 | – | – | – |
| Bdiaspc4_06505 | OmpW family protein | – | blr1311 | 6.0 | 44.9 | 23.3 | – | + |
| Bdiaspc4_07020 | ATP-dependent chaperone ClpB | clpB | blr1404 | 1.5 | 2.7 | 3.0 | – | – |
| Bdiaspc4_08825 | Nitrogenase molybdenum-iron protein alpha chain | nifD | blr1743 | 6.0 | 13.8 | 107.3 | + | – |
| Bdiaspc4_08830 | Nitrogenase molybdenum-iron protein subunit beta | nifK | blr1744 | 7.1 | 12.4 | 106.1 | + | – |
| Bdiaspc4_08835 | Nitrogenase iron-molybdenum cofactor biosynthesis protein NifE | nifE | blr1745 | 6.2 | 4.7 | 62.9 | + | – |
| Bdiaspc4_08840 | Nitrogenase iron-molybdenum cofactor biosynthesis protein NifN | nifN | blr1746 | 5.6 | 2.9 | 47.8 | + | – |
| Bdiaspc4_08845 | Nitrogen fixation protein NifX | nifX | blr1747 | 5.8 | – | 33.5 | + | – |
| Bdiaspc4_08880 | Hypothetical protein | – | bll1754 | 6.2 | 5.5 | 120.9 | – | – |
| Bdiaspc4_08885 | Iron-sulfur cluster assembly accessory protein | – | blr1755 | 5.0 | 7.0 | 138.7 | + | – |
| Bdiaspc4_08890 | Cysteine desulfurase NifS | nifS | blr1756 | 7.3 | 4.1 | 78.7 | – | – |
| Bdiaspc4_08895 | Putative nitrogen fixation protein NifT | nifT | bsr1757 | 5.6 | 4.8 | 105.4 | – | – |
| Bdiaspc4_08905 | Nitrogenase cofactor biosynthesis protein NifB | nifB | blr1759 | 5.8 | 2.9 | 74.1 | + | – |
| Bdiaspc4_08945 | OmpW family protein | – | bll1766 | 5.6 | 6.6 | 23.6 | – | + |
| Bdiaspc4_08960 | Nitrogenase iron protein | nifH | blr1769 | 7.9 | 7.0 | 96.2 | + | – |
| Bdiaspc4_08975 | Nitrogenase stabilizing/protective protein NifW | nifW | blr1771 | 5.4 | 2.2 | 95.2 | – | – |
| Bdiaspc4_08985 | Protein FixB | fixB | blr1773 | 6.0 | 2.2 | 47.6 | – | – |
| Bdiaspc4_08990 | Protein FixC | fixC | blr1774 | 5.8 | – | 38.1 | – | – |
| Bdiaspc4_09875 | Porin family protein | – | bll1944 | 8.4 | 3.8 | 89.7 | + | – |
| Bdiaspc4_10340 | SDR family oxidoreductase | fixR | blr2036 | 7.1 | – | 8.5 | – | – |
| Bdiaspc4_10345 | nif-specific transcriptional activator NifA | nifA | blr2037 | 6.6 | – | 3.2 | – | – |
| Bdiaspc4_10350 | Electron transfer flavoprotein subunit beta/FixAfamily protein | fixA | blr2038 | 5.9 | – | 31.9 | + | – |
| Bdiaspc4_10455 | Molecular chaperone GroEL | groEL3 | bll2059 | 5.6 | 2.9 | 47.4 | + | – |
| Bdiaspc4_10460 | Co-chaperone GroES | groES3 | bll2060 | 6.9 | 4.4 | 83.0 | + | – |
| Bdiaspc4_10475 | Flavin-dependent monooxygenase | nrgC | bll2063 | 5.2 | 4.4 | 105.0 | + | – |
| Bdiaspc4_10495 | Nodulate formation efficiency C protein | nfeC | bll2067 | 5.0 | – | 47.4 | + | – |
| Bdiaspc4_10745 | Non-ribosomal peptide synthetase | – | blr2108 | 6.5 | – | 39.0 | + | – |
| Bdiaspc4_10870 | Oxygenase | – | blr2131 | 5.5 | 15.9 | 298.2 | – | – |
| Bdiaspc4_10935 | Cytochrome P450 | cyp112 | blr2144 | 6.2 | 7.6 | 107.0 | + | – |
| Bdiaspc4_10940 | Cytochrome P450 BJ-3 | cyp114 | blr2145 | 6.5 | 3.3 | 55.0 | + | – |
| Bdiaspc4_10950 | Short-chain type dehydrogenase/reductase | – | blr2146 | 6.6 | – | 243.3 | – | – |
| Bdiaspc4_10955 | Cytochrome P450 BJ-4 | cyp117 | blr2147 | 6.2 | 2.4 | 26.4 | – | – |
| Bdiaspc4_12590 | Isocitrate lyase | aceA | blr2455 | 3.5 | 2.0 | – | – | – |
| Bdiaspc4_13350 | Universal stress protein | – | bll2590 | 3.1 | 11.1 | 5.2 | – | – |
| Bdiaspc4_14280 | Universal stress protein | – | blr2761 | 3.1 | 14.8 | 3.8 | – | + |
| Bdiaspc4_14295 | Cytochrome-c oxidase cbb3-type subunit II | ccoO/fixO | blr2764 | 3.9 | 47.0 | 26.8 | – | + |
| Bdiaspc4_14305 | cbb3-type cytochrome c oxidase subunit FixP | fixP | blr2766 | 5.6 | 43.7 | 23.9 | – | + |
| Bdiaspc4_14950 | 1,2-phenylacetyl-CoA epoxidase subunit A | ppaA | blr2891 | 4.6 | 9.8 | 6.1 | – | – |
| Bdiaspc4_18960 | NAD(P)-dependent alcohol dehydrogenase | – | blr3675 | 6.4 | – | 54.4 | – | – |
| Bdiaspc4_21300 | Cation acetate symporter | – | blr4115 | 4.9 | 21.9 | 12.3 | – | + |
| Bdiaspc4_21600 | Glutamine synthetase 2 | glnII | blr4169 | 2.0 | – | 2.1 | – | – |
| Bdiaspc4_24320 | Universal stress protein | – | bll4644 | 3.4 | 19.3 | – | – | – |
| Bdiaspc4_24375 | J domain-containing protein | dnaJ | blr4653 | 4.4 | 14.3 | – | – | – |
| Bdiaspc4_24405 | 1-phosphofructokinase family hexose kinase | – | blr4659 | 5.2 | 12.1 | – | – | – |
| Bdiaspc4_28005 | Host attachment protein | – | bll5315 | 2.9 | 15.0 | 5.9 | – | + |
| Bdiaspc4_31965 | MCE family protein | – | bll6063 | 2.2 | 10.5 | – | – | – |
| Bdiaspc4_31990 | GNAT family N-acetyltransferase | – | bll6068 | 4.3 | 5.4 | 2.3 | – | – |
| Bdiaspc4_32015 | Alpha/beta fold hydrolase | phaC2 | bll6073 | 3.3 | 13.5 | 4.1 | – | + |
| Bdiaspc4_35215 | Bacterioferritin | bfr | bll6680 | 1.7 | – | – | – | – |
| Bdiaspc4_36320 | Porin | – | bll6888 | 1.4 | – | 19.2 | – | – |
| Bdiaspc4_36645 | ModD protein | modD | bll6950 | 5.6 | – | 36.3 | – | – |
| Bdiaspc4_36650 | Molybdate ABC transporter substrate-binding protein | modA | blr6951 | 6.6 | 18.7 | 128.0 | + | – |
| Bdiaspc4_37130 | Periplasmic nitrate reductase subunit alpha | napA | blr7038 | 5.3 | 22.0 | 8.5 | – | + |
| Bdiaspc4_38745 | Hypothetical protein | – | blr7345 | 2.9 | 19.9 | 3.7 | – | + |
| Bdiaspc4_39840 | Hypothetical protein | – | bll7551 | 5.5 | 23.4 | 5.8 | – | – |
| Bdiaspc4_41200 | Hypothetical protein | – | bll7787 | 5.3 | 12.2 | 14.1 | – | + |
| Bdiaspc4_41905 | ABC transporter substrate-binding protein | – | bll7921 | 2.4 | – | 6.5 | – | – |
| Bdiaspc4_41910 | ABC transporter substrate-binding protein | – | blr7922 | 6.2 | – | 23.1 | – | – |
| Bdiaspc4_42205 | Dehydrogenase | – | bll7981 | 4.6 | 7.6 | 2.1 | – | + |
| Bdiaspc4_42210 | Class I SAM-dependent methyltransferase | – | bll7982 | 3.7 | 10.5 | 3.6 | – | + |
| Four proteins showing decreased expression in microoxic conditions in comparison to oxic conditions (p-value ≤ 0.2) | ||||||||
| Bdiaspc4_01330 | PQQ-dependent dehydrogenase, methanol/ethanol family | – | bll0333 | −0.8 | – | – | – | – |
| Bdiaspc4_05515 | Sugar ABC transporter substrate-binding protein | – | blr1123 | −3.0 | – | – | – | – |
| Bdiaspc4_36200 | Flagellin | fliC/lafA2 | bll6865 | −1.8 | – | – | – | – |
| Bdiaspc4_39525 | GMC Family oxidoreductase | – | blr7491 | −2.3 | – | – | – | – |
| Seventy-one genes/proteins showing increased expression in microoxic conditions in comparison to oxic conditions (log2 FC ≥ 1) at both trancriptional and protein levels not included above | ||||||||
| Bdiaspc4_01235 | TAT-dependent nitrous-oxide reductase | nosZ | blr0315 | 1.8 | 2.4 | – | – | – |
| Bdiaspc4_02185 | Hypothetical protein | – | blr0497 | 3.8 | 14.1 | 12.7 | – | + |
| Bdiaspc4_02350 | SDR family oxidoreductase | – | bll0527 | 1.1 | 2.9 | – | – | – |
| Bdiaspc4_06385 | Long-chain fatty acid-CoA ligase | – | blr1288 | 3.2 | 3.9 | 3.6 | – | – |
| Bdiaspc4_06390 | Oleate hydratase | – | blr1289 | 3.2 | 19.0 | 2.7 | – | + |
| Bdiaspc4_06420 | Aldo/keto reductase | – | bll1295 | 1.2 | 3.0 | – | – | – |
| Bdiaspc4_06685 | Hypothetical protein | – | bll1342 | 1.7 | 2.5 | – | – | – |
| Bdiaspc4_06740 | Amidohydrolase | – | blr1352 | 1.7 | 2.1 | – | – | – |
| Bdiaspc4_07460 | Sulfate ABC transporter substrate-binding protein | – | blr1482 | 1.2 | 3.2 | – | – | – |
| Bdiaspc4_08965 | Nitrogen fixation protein NifQ | nifQ | blr1770 | 4.6 | 3.2 | 85.0 | – | – |
| Bdiaspc4_09000 | Alkyl hydroperoxide reductase AhpD | ahpD | bll1776 | 4.7 | 4.1 | 78.6 | + | – |
| Bdiaspc4_09005 | Peroxiredoxin | ahpC | bll1777 | 4.5 | 7.8 | 169.8 | + | – |
| Bdiaspc4_09500 | Omptin family outer membrane protease | – | bll1872 | 4.7 | 4.2 | 115.4 | + | – |
| Bdiaspc4_09550 | RNA polymerase σ54 factor | rpoN1 | blr1883 | 4.4 | 3.9 | 7.8 | – | + |
| Bdiaspc4_09680 | GNAT family N-acetyltransferase | – | bll1906 | 4.3 | 8.3 | 120.0 | + | – |
| Bdiaspc4_10185 | Oxygen-independent coproporphyrinogen III oxidase | hemN1 | bll2007 | 4.5 | 17.3 | 29.1 | – | + |
| Bdiaspc4_10960 | Polyprenyl synthetase family protein | – | blr2148 | 4.6 | 4.2 | 25.4 | – | – |
| Bdiaspc4_11365 | Aspartate aminotransferase family protein | – | blr2221 | 1.5 | 2.9 | – | – | – |
| Bdiaspc4_12935 | Phosphoketolase family protein | – | bll2518 | 4.3 | 8.2 | – | – | – |
| Bdiaspc4_14265 | Response regulator | – | bll2758 | 4.8 | 5.5 | 2.4 | – | – |
| Bdiaspc4_14285 | CBS domain-containing protein | – | blr2762 | 4.8 | 13.2 | 3.1 | – | – |
| Bdiaspc4_14310 | Cytochrome c oxidase accessory protein CcoG | ccoG/fixG | blr2767 | 4.3 | 32.5 | 13.0 | – | + |
| Bdiaspc4_14320 | Copper-translocating P-type ATPase | fixI | blr2769 | 3.8 | 23.5 | 11.0 | – | + |
| Bdiaspc4_14930 | Phasin | – | blr2887 | 1.8 | 2.4 | 3.4 | – | – |
| Bdiaspc4_14960 | Phenylacetate-CoA oxygenase subunit PaaI | paaI | blr2893 | 2.1 | 9.3 | 5.6 | – | – |
| Bdiaspc4_14970 | Phenylacetate-CoA oxygenase/reductase subunit PaaK | paaK | blr2895 | 1.9 | 5.0 | 2.6 | – | – |
| Bdiaspc4_14980 | Phenylacetate-CoA ligase | paaF | blr2897 | 2.0 | 4.5 | – | – | – |
| Bdiaspc4_16100 | MBL fold metallo-hydrolase | – | bll3115 | 2.9 | 15.4 | – | – | – |
| Bdiaspc4_16105 | Ribose-phosphate pyrophosphokinase | – | bll3116 | 4.4 | 7.7 | – | – | – |
| Bdiaspc4_16110 | Thymidine phosphorylase family protein | – | bll3117 | 2.1 | 5.1 | – | – | – |
| Bdiaspc4_19720 | HAD family hydrolase | – | blr3815 | 3.7 | 5.8 | – | – | – |
| Bdiaspc4_20685 | NAD-dependent succinate-semialdehyde dehydrogenase | – | bll3998 | 2.6 | 28.1 | 8.4 | – | + |
| Bdiaspc4_21285 | CusA/CzcA family heavy metal efflux RND transporter | – | blr4112 | 4.8 | 6.4 | – | – | – |
| Bdiaspc4_21700 | Hypothetical protein | – | bsl4187 | 4.5 | 2.3 | – | – | – |
| Bdiaspc4_22005 | Pyridoxamine 5'-phosphate oxidase family protein | – | blr4240 | 3.8 | 12.5 | – | – | – |
| Bdiaspc4_22345 | Amidase | – | bll4303 | 1.6 | 3.9 | – | – | – |
| Bdiaspc4_22980 | Translational machinery protein | – | bll4412 | 2.6 | 6.6 | – | – | – |
| Bdiaspc4_24325 | Host attachment protein | – | bll4645 | 3.2 | 21.8 | – | – | – |
| Bdiaspc4_24330 | CBS domain-containing protein | – | blr4646 | 3.2 | 28.1 | – | – | – |
| Bdiaspc4_24365 | Protein-L-isoaspartate(D-aspartate) O-methyltransferase | – | bll4651 | 4.6 | 28.7 | 9.7 | – | + |
| Bdiaspc4_24370 | Nitroreductase | – | blr4652 | 2.9 | 51.6 | 5.9 | – | + |
| Bdiaspc4_24385 | Phosphoenolpyruvate synthase | – | blr4655 | 4.3 | 11.2 | 2.0 | – | – |
| Bdiaspc4_24400 | Glucokinase | glk | blr4658 | 3.7 | 9.4 | 2.9 | – | – |
| Bdiaspc4_27515 | Co-chaperone GroES | groES1 | blr5226 | 3.4 | 2.1 | – | – | – |
| Bdiaspc4_29305 | CBS domain-containing protein | – | bll5551 | 1.1 | 2.0 | – | – | – |
| Bdiaspc4_29865 | Alcohol dehydrogenase AdhP | adhP | bll5655 | 2.8 | 18.0 | 3.9 | – | + |
| Bdiaspc4_30480 | Efflux RND transporter permease subunit | – | bll5771 | 3.8 | 2.6 | – | – | – |
| Bdiaspc4_30485 | Efflux RND transporter periplasmic adaptor subunit | – | bll5772 | 4.0 | 3.5 | – | – | – |
| Bdiaspc4_30510 | DUF302 domain-containing protein | – | blr5777 | 4.3 | 5.0 | 3.3 | – | – |
| Bdiaspc4_30515 | Cytochrome c oxidase accessory protein CcoG | ccoG/fixG | blr5778 | 3.4 | 4.6 | 4.1 | – | – |
| Bdiaspc4_31945 | Cyclase family protein | – | blr6059 | 1.5 | 2.6 | – | – | – |
| Bdiaspc4_31950 | CRP/FNR family transcriptional regulator | – | bll6060 | 1.3 | 2.3 | 2.2 | – | – |
| Bdiaspc4_31970 | ABC transporter ATP-binding protein | – | bll6064 | 2.8 | 4.6 | 2.1 | – | – |
| Bdiaspc4_31975 | MlaE family lipid ABC transporter permease subunit | – | bll6065 | 3.4 | 6.7 | – | – | – |
| Bdiaspc4_31995 | Universal stress protein | – | bll6069 | 2.7 | 18.5 | 7.5 | – | + |
| Bdiaspc4_32020 | CBS domain-containing protein | – | blr6074 | 2.6 | 35.6 | 4.7 | – | + |
| Bdiaspc4_34005 | Methyltransferase | – | bll6449 | 1.4 | 2.7 | – | – | – |
| Bdiaspc4_34035 | ABC transporter substrate-binding protein | – | bll6455 | 2.8 | 4.4 | – | – | – |
| Bdiaspc4_34375 | Aryl-sulfate sulfotransferase | – | bsr6521 | 2.6 | 3.4 | – | – | – |
| Bdiaspc4_36795 | Chaperonin GroEL | groEL2 | blr6979 | 1.6 | 3.9 | 2.0 | – | – |
| Bdiaspc4_37135 | Nitrate reductase cytochrome c-type subunit | napB | blr7039 | 2.8 | 47.4 | 22.6 | – | – |
| Bdiaspc4_37380 | CRP/FNR family transcriptional regulator | nnrR | blr7084 | 3.6 | 7.1 | – | – | – |
| Bdiaspc4_37390 | Oxygen-independent coproporphyrinogen III oxidase | hemN2 | bll7086 | 4.3 | 29.4 | 7.3 | – | + |
| Bdiaspc4_37770 | DUF2852 domain-containing protein | – | bll7160 | 2.5 | 2.1 | 4.9 | – | – |
| Bdiaspc4_39110 | Elongation factor G | – | bll7414 | 1.9 | 4.1 | 2.8 | – | – |
| Bdiaspc4_40040 | Indolepyruvate ferredoxin oxidoreductase family protein | – | blr7589 | 1.1 | 3.6 | – | – | – |
| Bdiaspc4_40955 | Molecular chaperone | – | blr7740 | 3.2 | 2.1 | 4.5 | – | – |
| Bdiaspc4_41165 | Hypothetical protein | – | blr7780 | 4.5 | 8.6 | 17.0 | – | – |
| Bdiaspc4_41645 | HlyD family efflux transporter periplasmic adaptor subunit | – | blr7872 | 3.5 | 14.1 | – | – | – |
| Bdiaspc4_42105 | Hsp20/alpha crystallin family protein | – | blr7961 | 4.8 | 28.4 | 25.2 | – | + |
| Bdiaspc4_43115 | HugZ family protein | – | bll8143 | 3.2 | 2.2 | – | – | – |
Shown are also 71 genes/proteins; i.e., 117 genes/proteins comprising the “expanded microoxia-induced transcriptome/proteome” (log2 fold change ≥ 1 at both transcriptional and protein level) minus 46 genes/proteins included in the “core microoxic proteome.”
a
Nomenclature of B. diazoefficiens 110spc4 genes according to the NCBI annotation (GenBank acc. # CP032617); this work.
b
Protein/gene product according to the NCBI annotation (GenBank acc. # CP032617); this work.
c
Gene name according to the NCBI annotation with modifications shaded in gray (GenBank acc. # CP032617); this work.
d
Best blast hit in the B. diazoefficiens USDA 110 genome (Kaneko et al., 2002; GenBank acc. # NC_004463.1; RefSeq annotation as from January 2016).
e
Log2 fold change (FC) values from the comparison of wild-type cells grown microoxically (0.5% O2) in comparison with those of cells grown oxically in proteomics experiments.
f
FC values from the comparison of wild-type cells grown microoxically (0.5% O2) in comparison with those of cells grown oxically in transcriptomics experiments (Pessi et al., 2007). – indicates the gene was not differentially expressed.
g
FC values from the comparison of wild-type soybean bacteroids in comparison with those of wild-type cells grown oxically in transcriptomics experiments (Pessi et al., 2007). – indicates the gene was not differentially expressed.
h
The gene belongs to the defined NifA + RpoN1+2 regulon according to Hauser et al. (2007). +, yes; –, not.
i
The gene is part of the direct FixK2-dependent regulon as defined by Mesa et al. (2008). +, yes; –, not.