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. 2020 May 9;12(5):310. doi: 10.3390/toxins12050310

Table 2.

BMAA action on selected identified proteins based on the statistical significance of the observed differences in protein profile of Nostoc during nitrogen starvation.

No. Protein Gene Function Fold Regulation * p-Value
LFQ Ratio
BMAA Treated Sample/Control Sample
Nitrogen metabolism (3 proteins)
1 nrtA alr0608 nitrate-binding protein 1.76 0.002
2 glnB|P-II all2319 nitrogen regulatory protein 0.55 0.09
3 nifD all1454 molybdenum-iron protein subunit alpha in nitrogenase 0.54 0.047
Heterocyst formation (two DNA-binding proteins)
4 Apb2 all1939 transcription regulation of hepA and hepC genes 0.63 0.08
5 Abp1 all1940 transcription regulation of hepA and hepC genes 1.49 0.078
Nucleotides metabolism, purine and pyrimidine (4 proteins)
6 EC:2.7.4.6
nucleoside diphosphate kinase
alr3402 transferring phosphorus-containing groups 0.75 0.004
7 EC:2.1.2.2
phosphoribosylglycinamide formyltransferase-2
alr1299 purine metabolism 2.14 0.05
8 EC:2.1.2.3 3.5.4.10 | purH; bifunctional purine biosynthesis protein all3093 purine metabolism 0.71 0.08
9 EC:1.1.1.205
inosine 5-monophosphate dehydrogenase
alr0051 purine metabolism 1.75 0.00013
Secondary metabolites (4 proteins)
10 EC:2.2.1.7
1-deoxy-xylulose 5-phosphate synthase
alr0599 Thiamine metabolism; Terpenoid backbone biosynthesis found only in control sample 0.00001
11 EC:2.8.1.10 | thiG
thiazole synthase
all3519 Thiamine biosynthesis protein found only in control sample 0.02
12 EC:1.17.7.1 1.17.7.3 | ispG
4-hydroxy-3-methylbut-2-en-1-yl diphosphate synthase
all2501 Terpenoid backbone biosynthesis 0.55 0.0012
13 EC:1.3.1.83 1.3.1.111 | chlP
geranylgeranyl hydrogenase
alr0128 Porphyrin and chlorophyll metabolism;
Terpenoid backbone biosynthesis
0.49 0.01
Photosynthesis (9 proteins)
14 psaA
photosystem I P700 chlorophyll a apoprotein A1
alr5154 photosystem I 0.38 0.01
15 petC
cytochrome b6-f complex iron-sulfur subunit
all2453 cytochrome b6-f 1.75 0.024
16 psbW
photosystem II 13kDa protein
all0801 photosystem II found only in BMAA treated sample 0.04
17 petE
plastocyanin
all0258 plastocyanin 0.58 0.06
18 cpcA
phycocyanin alpha chain
alr0529 phycocyanin 0.56 0.075
19 apcD
allophycocyanin B alpha chain
all3653 allophycocyanin 0.82 0.076
20 EC:4.2.1.24
delta-aminolevulinic acid dehydratase
alr4380 Porphyrin and chlorophyll metabolism 0.51 0.08
21 psaB
photosystem I P700 chlorophyll a apoprotein A2
alr5155 photosystem I 0.26 0.08
22 psaF
photosystem I subunit III
all0109 photosystem I 0.61 0.04
ABC-transporters and transporters (3 proteins)
23 branched-chain amino acid transport system substrate-binding protein alr2535 ABC transporters; Quorum sensing 0.59 0.00003
24 secY | preprotein translocase subunit all4197 Quorum sensing found only in control sample 0.03
25 peptide/nickel transport system substrate-binding protein alr0140 periplasmic oligopeptide-binding ABC transporter
Quorum sensing
1.61 0.038
Amino acids metabolism (8 protein)
26 EC 4.3.1.19
threonine dehydratase
alr4232 Glycine, serine and threonine metabolism;
Valine, leucine and isoleucine biosynthesis
found only in control sample 0.0008
27 EC 2.6.1.52
phosphoserine aminotransferase
all1683 Glycine, serine and threonine metabolism;
Cysteine and methionine metabolism
0.62 0.01
28 EC 2.5.1.47
cysteine synthase A
alr4416 Cysteine and methionine metabolism 0.69 0.03
29 EC 2.3.3.13
leuA
2-isopropylmalate synthase
alr4840 Valine, leucine and isoleucine biosynthesis;
Pyruvate metabolism
0.55 0.06
30 ureC
urease subunit alpha
alr3670 Arginine biosynthesis;
Purine metabolism
0.82 0.08
31 EC:2.6.1.16 | NodM
glutamine--fructose-6-phosphate aminotransferase
alr3464 Alanine, aspartate and glutamate metabolism 2.20 0.002
32 EC:1.2.1.16 1.2.1.79 1.2.1.20
succinate-semialdehyde dehydrogenase / glutarate-semialdehyde dehydrogenase
all3556 Alanine, aspartate and glutamate metabolism; Lysine degradation 1.64 0.022
33 thrA
homoserine dehydrogenase
all4120 Glycine, serine and threonine metabolism 1.73 0.05
Chaperones (3 proteins)
34 dnaK
molecular chaperone DnaK
alr2990 Folding, sorting and degradation found only in BMAA treated sample 0.002
35 dnaK
molecular chaperone DnaK
alr1742 Folding, sorting and degradation 1.23 0.09
36 groES
co-chaperonin GroES
alr3661 Chaperones and folding catalysts 1.54 0.08
Signalling, Stress response, GTP-binding proteins and proteases (8 proteins)
37 TypA all4140 GTP-binding protein
Ribosome –binding
Stress responce
2.04 0.059
38 peroxiredoxin alr4641 signaling and cellular processes; acting on a peroxide as acceptor 2.02 0.0015
39 EC:1.15.1.1
superoxide dismutase, Fe-Mn family
all0070 Acting on superoxide as acceptor found only in BMAA treated sample 0.0028
40 EC:1.8.1.7
gor; glutathione reductase (NADPH)
all4968 Glutathione metabolism 1.45 0.047
41 EC:1.8.1.9
thioredoxin reductase
all0737 Selenocompound metabolism 2.22 0.07
42 AhpC/TSA family protein alr4404 This family includes peroxiredoxin proteins 0.39 0.035
43 cyclic-di-GMP-binding protein all4662 signaling and cellular processes 0.73 0.05
44 EC:3.4.24. | ftsH
cell division protease
all4936 cell division protease FtsH 1.89 0.015
Translation (4 proteins)
45 GTP-binding protein LepA all2508 elongation factor found only in control sample 0.05
46 EC:6.1.1.17
gltX | glutamyl-tRNA synthetase
all3205 Aminoacyl-tRNA biosynthesis;
Porphyrin and chlorophyll metabolism
found only in control sample 0.005
47 ribosome recycling factor (rrf) alr1208 Translation factors 1.37 0.086
48 EC:6.1.1.6 lysS
lysyl-tRNA synthetase
all4071 Aminoacyl-tRNA biosynthesis 1.28 0.096
Ribosomal proteins, (5 proteins)
49 rplX | 50S
ribosomal protein L24
asl4204 genetic information processing 2.56 0.014
50 rpsJ | 30S
ribosomal protein S10
all4336 genetic information processing 0.068 0.059
51 rpsF | 30S
ribosomal protein S6
all4802 genetic information processing 1.27 0.06
52 rps7 | 30S
ribosomal protein S7
all4339 genetic information processing 0.74 0.06
53 rplL | 50S
ribosomal protein L7/L12
alr5303 genetic information processing 0.67 0.094
Transcription (3 proteins)
54 EC:2.7.7.6 rpoB
DNA-directed RNA polymerase subunit beta
alr1594 Transcription 1.52 0.05
56 EC:2.7.7.6 rpoC1
DNA-directed RNA polymerase subunit beta
alr1595 Transcription machinery 2.13 0.08
55 sigA | RNA
polymerase sigma factor RpoD
all5263 Transcription;
Transcription regulation;
DNA-binding
0.39 0.0046
DNA metabolism (4 proteins)
57 EC:5.6.2.2 DNA gyrase subunit A all0860 DNA replication
DNA repair and recombination
1.92 0.02
58 recA
recombinase A
all3272 DNA repair and recombination 3.03 0.047
59 EC:5.6.2.2 gyrB
DNA gyrase subunit B
all5265 Enzymes altering DNA conformation 1.56 0.08
60 nucA
sugar-non-specific nuclease
all7362;
alr8011
genetic information processing 2.63 0.08
CO2 fixation and CO2-concentrating mechanism (two proteins)
61 rbcL EC:4.1.1.39
ribulose bisophosphate carboxylase
alr1524 Carbon metabolism 0.67 0.0008
62 ccmM
carbon dioxide concentrating mechanism protein
all0865 Carbon metabolism 0.64 0.02
Carbohydrate metabolism, Glycolisis and gluconeogenesis (6 proteins)
63 EC:2.7.2.3 phosphoglycerate kinase (pgk) all4131 Glycolysis
Gluconeogenesis
0.78 0.0008
64 nucleotide sugar epimerase all3509 Sugar metabolism 0.59 0.07
65 EC:3.1.3.11
fructose-1,6-bisphosphatase I
all4021 Glycolysis
Gluconeogenesis
0.76 0.006
66 EC:1.1.1.44 1.1.1.343
6-phosphogluconate dehydrogenase
alr5275 Pentose phosphate pathway, Glutathione metabolism 0.68 0.05
67 NADH-dependent butanol dehydrogenase alr4566 Propanoate metabolism 0.73 0.05
68 Phosphoglucomutase all5089 Glycogenolysis and Gluconeogenesis 0.77 0.057

* Fold regulation stands for BMAA/control ratio as it was done in [17], i.e., fold changes between BMAA-treated and control samples are shown (p < 0.1). Additional information about 164 identified BMAA-regulated proteins, whose fold regulation was detected with 0.1 < p < 1 (not significant) and with, N.A. i.e. not available value, because only in one or two sample replications the peptide was detected, thereby p-value could not be calculated, is presented in Tables S4 and S5, as a Supplementary.