Oxidative Phosphorylation for Aerobic Survival, but Not for Growth: The Peculiar ‘Make-Accumulate-Consume’ Strategy in Zymomonas mobilis
Abstract
:1. Introduction
2. Materials and Methods
2.1. Plasmid and Strain Construction
2.2. Cultivation, Starvation and Assessment of Viability
2.3. Cultivation of EGFP-Bearing Strains in the Microplate Reader and Monitoring of EGFP Fluorescence
2.4. FTIR Spectroscopy of Biomass
2.5. Preparation of Cytoplasmic Membranes and Respiratory Chain NADH Oxidase Assay
3. Results
3.1. The Impact of Respiratory Chain Activity on the Viability of Non-Growing Z. mobilis Cells
3.2. Expression of the Respiratory Chain Complexes under Ethanol Stress
4. Discussion
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
Appendix A
Gene/Operon Names, and Sequence i.d. | Sequences of the Amplified Chromosomal Regions, Bearing the Promoters of the Respective Genes/Operons (5’ → 3’) | Forward and Reverse Primer Sequences (5’ → 3’) |
---|---|---|
Cytochrome c peroxidase perC ZZ6_0192 | →ZZ6_0191 CCGATGAATGGGTAAAATAAGACCTTTTCCCTTTCTAAAATTTCAGAGGTGGCTTTATTC CTGTTAAAGCCACCTTTTATTTTATCTTTTTCTTTATTCTTTCTCAGCTTTTCTGATTAA AAAATTTTGTAAATATAGCCAATATTTCCAATGAAATATCAGGTTAAAATATCTGTAAAG AACGAGAATTTTCTTATCACTTTAATGATAACTATTGGCATCATCAAAATCATCAAGAAT TAATCAAAATTGAAATGACAGTTATGCCTTTTACTCTAAAAGGGATGTGCTTTCTGTCTT GGAATAAGGCCATATTTTTGTTAATTCACAATAAATAAAAAGGTAAATCATCTTCAATAG GGAATCGGATACTATAAATTTATAGCCGACCATCCGATCATCTCTGGCGCTGGATTAAGA TAACGAGGGGCAAGCACAGTTTTATGAATATCAAGGCTTTATT →ZZ6_0192 | F primer BamHI CCGATGAATGGGATCCATAAGACCTTTTCC |
R primer EcoRI AGCCTTGATATTCATGAATTCGTGCTTGCC | ||
Cytochrome bc1 (ubiquinol:cytc oxidoreductase) operon: FeS cluster (Rieske) subunit ZZ6_0349; Cyt b subunit ZZ6_0348; Cyt c1 subunit ZZ6_0347 | → ZZ6_0350 CTCGCCGCAACCGTCTTGTTCTGGCTATGAGTCCTGAGCCTAGATTTCATGATAGTCAAT ATATTAAAAAATTATATATTGTAGTAATCTTTCTTAAAAAATCAGAATAATTGATTTAAA TATCATTAATTATGGCATTTTAATTATCATTTTTAATATTTTCATGGACAATGAAGAAAA CTTATTATGTTTTTATTGTAGTAAGCGTTGCAAAAAATATTGTAAGTAATTTACAGTAGA GTAGGTTCGTCAAGGGATATGAAGAATAGCGAAGCGAA → ZZ6_0349 | F primer BamHI TTGTTCTGGCTATGGATCCTGAGCCTAGAT |
R primer EcoRI TTCGCTATTCTTCATGAATTCTGACGAACC | ||
Cytochrome bd operon: cydA ZZ6_1532; cydB ZZ6_1531 | ZZ6_1533 ← TCAAGGGTGGAAATGGTCATGTCGCTTCAACCTTTGATTCTATGAGCGAGGAAAGACTTA GGAGATATATCTAACAAAATTCGACCCGATCTGACAGCTATTATTAAAATGCAGAATAAG GTCGCGGGCTTTTTATCAGCTAACTCTAACAAAAAACAGAATCATTCGAAAAAGAATAAT AGAATACTCTATATTTAAATTATAAATTGATCCTTTTTCATATGGCTTTTTAATCACAAC CGCCCTAAAATCGGAAAATATCTGTTCCCTTGGGTGGTCTGTTATCAGAGATAGAAAATA ATTCGATTTCAAAAATCGTTATTTTCAATATTGAGACCTAAGCCCCTTTTCCCTTGTTCC TATCGTGACTTTCTTTTGAAATCGCCCCTATTCAACGAATTTAGGGGCAAGTTTTAAAAT AAAGCCCTTAATCGCTTCATCACTATTTTATTTAAAAAATGTTATTGATCTATAAAAAGA TACTATAACTACAGCAATATACTCAAAACAATCTGACATGGTCATATTAAATTTTAAAAT TTATCAAAAAAATAATTAAAATTAAAGAAATATAAAACGATAATTAAACCCAATTGAAGA TAAATAGACTGTAGATAGAGATTATTACCCCCGAGGATCAAGAAATTCTCTATTGACACA ACACCCGATGCTATCAATACACCGATAATATATAGGGGGCATTTTACAGATTCAGGAAGC TGATCCCTGAAGAAAAGCCCGTAGACCCTAATAATTCCTAATATTATCGACGGAGCCATT TCTATGGTACCAGATGCGACCGC → ZZ6_1532 | F primer BamHI GGTGGAAATGGATCCGTCGCTTCAACCTTT |
R primer EcoRI CGCATCTGGTACCATGAATTCGGCTCCGTC | ||
Type II NADH: ubiquionone oxidoreductase ndh ZZ6_0213 | ZZ6_0214 ← TGATCGGTTTGTTTTTCCATAACCCATATTGACGGGAAAAGAAGCCAAAGGTCAATCAGA GAAAGCGCGCTTTAAACAAAGCCCATGAGGATGATCAAAGACAGAGACCGGATAAGGGCA AAGATAGTTTCACAGTAAGCAATAAAAACTTTCACTCTGACTTATAATTTATGTGAAACA GATTTGAATGTTCTTCGTTAGTTACAGCAAAAGGTAATTGAGGCGGCTCGCAAACCACCA CGCCAAAGGGGGCTGGGTCGCTTGGAAGAGAATAGAGGTTTCAAATGTCGAAGAATGGTA → ZZ6_0213 | F primer BamHI GGTTTGTGGATCCATAACCCATATTGACGG |
R primer EcoRI GACATGAATTCCCTCTATTCTCTTCCAAGC | ||
EGFP gene in plasmid pQE-EGFP egfp | → egfp ATACGGATCCACCGGTCGCCACCATGGTGAGCAAGGGCGAGGAGCTGTTCACCGGGGTGGTGCCCATCCTGGTCGAGCTGGACGGCGACGTAAACGGCCACAAGTTCAGCGTGTCCGGCGAGGGCGAGGGCGATGCCACCTACGGCAAGCTGACCCTGAAGTTCATCTGCACCACCGGCAAGCTGCCCGTGCCCTGGCCCACCCTCGTGACCACCCTGACCTACGGCGTGCAGTGCTTCAGCCGCTACCCCGACCACATGAAGCAGCACGACTTCTTCAAGTCCGCCATGCCCGAAGGCTACGTCCAGGAGCGCACCATCTTCTTCAAGGACGACGGCAACTACAAGACCCGCGCCGAGGTGAAGTTCGAGGGCGACACCCTGGTGAACCGCATCGAGCTGAAGGGCATCGACTTCAAGGAGGACGGCAACATCCTGGGGCACAAGCTGGAGTACAACTACAACAGCCACAACGTCTATATCATGGCCGACAAGCAGAAGAACGGCATCAAGGTGAACTTCAAGATCCGCCACAACATCGAGGACGGCAGCGTGCAGCTCGCCGACCACTACCAGCAGAACACCCCCATCGGCGACGGCCCCGTGCTGCTGCCCGACAACCACTACCTGAGCACCCAGTCCGCCCTGAGCAAAGACCCCAACGAGAAGCGCGATCACATGGTCCTGCTGGAGTTCGTGACCGCCGCCGGGATCACTCTCGGCATGGACGAGCTGTACAAGTAAGGAGGTTCCCGCGGA | F primer EcoRI ATACGGATCCACCGGTCGAATTCATGGTGA |
R primer HindIII TCCGCGGGAAAGCTTTTACTTGTACAGCTC |
Appendix B
Incubation without Substrate Addition | Carbohydrates | Nucleic Acids | Proteins | Lipids | ||||
---|---|---|---|---|---|---|---|---|
0 h | 6 h | 0 h | 6 h | 0 h | 6 h | 0 h | 6 h | |
Mean value | 12.65 | 11.97 | 17.57 | 18.45 | 57.74 | 57.71 | 2.05 | 1.87 |
±SEM | ±0.47 | ±0.39 | ±0.35 | ±0.61 | ±0.61 | ±0.27 | ±0.24 | ±0.17 |
p value | 0.33 | 0.28 | 0.97 | 0.55 | ||||
Incubation with 1 g L−1 glucose additions, once per hour | ||||||||
Mean value | 12.70 | 12.21 | 15.93 | 15.48 | 59.13 | 60.06 | 2.24 | 2.25 |
±SEM | ±0.87 | ±0.39 | ±0.19 | ±0.15 | ±0.68 | ±0.49 | ±0.36 | ±0.10 |
p value | 0.63 | 0.11 | 0.31 | 0.98 |
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Plasmid/Strain | Characteristics | Source |
---|---|---|
pBBR1MCS-2 | Plasmid vector, kanr | Addgene |
pNdh | pBBR1MCS-2 derivative with a 1.55 kb insert between the HindIII and BamHI sites of its MCS, containing the ORF of the type II respiratory NADH dehydrogenase (ndh, gene ZZ6_0213) together with its native promoter | [23] |
pQE-EGFP | pQE-30 plasmid with a 0.72 kb insert of the EGFP coding sequence in the MCS | Addgene |
pBBR-EGFP | pBBR1MCS-2 derivative with a 0.72 kb insert of the EGFP coding sequence in the MCS between EcoRI and HindIII restriction sites | Present work |
pBBR:Pndh-EGFP | pBBR-EGFP derivative with a 0.26 kb insert, containing the promoter region of the type II respiratory NADH dehydrogenase (ndh, gene ZZ6_0213), upstream of the EGFP coding sequence in the MCS between BamHI and EcoRI restriction sites | Present work |
pBBR:Pbc1-EGFP | pBBR-EGFP derivative with a 0.23 kb insert, containing the promoter region of the cytochrome bc1 operon (genes ZZ6_0349, ZZ6_0348, ZZ6_0347), upstream of the EGFP coding sequence in the MCS between BamHI and EcoRI restriction sites | Present work |
pBBR:Pbd-EGFP | pBBR-EGFP derivative with a 0.76 kb insert, containing the promoter region of the cytochrome bd operon (cydAB; genes ZZ6_1532, ZZ6_1531), upstream of the EGFP coding sequence in the MCS between BamHI and EcoRI restriction sites | Present work |
pBBR:PperC-EGFP | pBBR-EGFP derivative with a 0.42 kb insert, containing the promoter region of the cytochrome c peroxidase (perC, gene ZZ6_0192), upstream of the EGFP coding sequence in the MCS between BamHI and EcoRI restriction sites | Present work |
Zm6 | Wild type, parent strain | ATCC 29191 |
Zm6-ndh | Zm6 with a Cmr (chloramphenicol acetyltransferase gene) inserted in the AgeI site of the chromosomal ORF of its ndh | [17] |
Zm6-ndh_pNdh | Zm6-ndh transformed with plasmid pNdh | [23] |
Zm6_pBBR-EGFP | Zm6 transformed with plasmid pBBR-EGFP | Present work |
Zm6_pBBR:Pndh-EGFP | Zm6 transformed with plasmid pBBR:Pndh-EGFP | Present work |
Zm6_pBBR:Pbc1-EGFP | Zm6 transformed with plasmid pBBR:Pbc1-EGFP | Present work |
Zm6_pBBR:Pbd-EGFP | Zm6 transformed with plasmid pBBR:Pbd-EGFP | Present work |
Zm6_pBBR:PperC-EGFP | Zm6 transformed with plasmid pBBR:PperC-EGFP | Present work |
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Strazdina, I.; Bikerniece, M.; Paegle, E.R.; Shvirksts, K.; Grube, M.; Lasa, Z.; Rutkis, R.; Kalnenieks, U. Oxidative Phosphorylation for Aerobic Survival, but Not for Growth: The Peculiar ‘Make-Accumulate-Consume’ Strategy in Zymomonas mobilis. Fermentation 2023, 9, 951. https://doi.org/10.3390/fermentation9110951
Strazdina I, Bikerniece M, Paegle ER, Shvirksts K, Grube M, Lasa Z, Rutkis R, Kalnenieks U. Oxidative Phosphorylation for Aerobic Survival, but Not for Growth: The Peculiar ‘Make-Accumulate-Consume’ Strategy in Zymomonas mobilis. Fermentation. 2023; 9(11):951. https://doi.org/10.3390/fermentation9110951
Chicago/Turabian StyleStrazdina, Inese, Mara Bikerniece, Evelina Rezija Paegle, Karlis Shvirksts, Mara Grube, Zane Lasa, Reinis Rutkis, and Uldis Kalnenieks. 2023. "Oxidative Phosphorylation for Aerobic Survival, but Not for Growth: The Peculiar ‘Make-Accumulate-Consume’ Strategy in Zymomonas mobilis" Fermentation 9, no. 11: 951. https://doi.org/10.3390/fermentation9110951