Why organelle genomes? Costs and benefits of DNA in mitochondria and chloroplasts
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1 School of Chemistry and Molecular Biosciences University of Queensland 18th February 2009 Why organelle genomes? Costs and benefits of DNA in mitochondria and chloroplasts John F. Allen Australian Academy of Science Rudi Lemberg Travelling Fellow School of Biological and Chemical Sciences, Queen Mary, University of London jfallen.org 1
2 Max Rudolph Lemberg
3 Genes in organelles
4 a chloroplast Christmas-Rose leaf SEM cross-section; Science Photo Library (SPL)
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6 Mitochondria (singular; mitochondrion).
7 Mitochondria (singular; mitochondrion). mitochondria power animal and plant cells
8 Mitochondria (singular; mitochondrion). mitochondria power animal and plant cells mitochondria are domesticated bacteria
9 Mitochondria (singular; mitochondrion). mitochondria power animal and plant cells mitochondria are domesticated bacteria during domestication - cell evolution - these bacteria relinquished many genes to the nucleus of the host cell...
10 Mitochondria (singular; mitochondrion). mitochondria power animal and plant cells mitochondria are domesticated bacteria during domestication - cell evolution - these bacteria relinquished many genes to the nucleus of the host cell.... and there are now few left (13 in the case of vertebrates, including mammals, including humans) encoding around 1 % of mitochondrial proteins
11 Mitochondria (singular; mitochondrion). mitochondria power animal and plant cells mitochondria are domesticated bacteria during domestication - cell evolution - these bacteria relinquished many genes to the nucleus of the host cell.... and there are now few left (13 in the case of vertebrates, including mammals, including humans) encoding around 1 % of mitochondrial proteins And it is always the same 1 % (more or less)...
12 Mitochondria (singular; mitochondrion). mitochondria power animal and plant cells mitochondria are domesticated bacteria during domestication - cell evolution - these bacteria relinquished many genes to the nucleus of the host cell.... and there are now few left (13 in the case of vertebrates, including mammals, including humans) encoding around 1 % of mitochondrial proteins And it is always the same 1 % (more or less)... Why?
13 Comparison of mitochondrial genomes Less complex mitochondrial genomes encode subsets of the proteins and ribosomal RNAs that are encoded by larger mitochondrial genomes. There are only four genes present in all known mitochondrial genomes; these encode ribosomal RNAs (rns and rnl), cytochrome b (cob), and a cytochrome oxidase subunit (cox1). (Adapted from M.W. Gray et al., Science 283: , With permission from AAAS.)
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15 Inter-membrane space I II III IV ase Mitochondrial matrix
16 Inter-membrane space I II III IV ase H + H + H + H + NADH O 2 H 2 O NAD + succinate fumarate ADP Mitochondrial matrix
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18 Cytosol Mitochondrial matrix
19 Why mitochondria have genomes
20 Why mitochondria have genomes Problem: Why are there genes in mitochondria?
21 Why mitochondria have genomes Problem: Why are there genes in mitochondria? Proposed solution (hypothesis): The location has an advantage, since energy conversion, in order to be both safe and efficient, requires a set of proteins whose genes reside with them, in the same compartment of the cell.
22 Why mitochondria have genomes Problem: Why are there genes in mitochondria? Proposed solution (hypothesis): The location has an advantage, since energy conversion, in order to be both safe and efficient, requires a set of proteins whose genes reside with them, in the same compartment of the cell. CoRR - Co-Location for Redox* Regulation.
23 Why mitochondria have genomes Problem: Why are there genes in mitochondria? Proposed solution (hypothesis): The location has an advantage, since energy conversion, in order to be both safe and efficient, requires a set of proteins whose genes reside with them, in the same compartment of the cell. CoRR - Co-Location for Redox* Regulation. CoRR applies equally to mitochondria and chloroplasts
24 Why mitochondria have genomes Problem: Why are there genes in mitochondria? Proposed solution (hypothesis): The location has an advantage, since energy conversion, in order to be both safe and efficient, requires a set of proteins whose genes reside with them, in the same compartment of the cell. CoRR - Co-Location for Redox* Regulation. CoRR applies equally to mitochondria and chloroplasts *Redox reactions are chemical reaction in which an electron is transferred from one molecule to another - the basis of biological energy conversion.
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26 Bacterium
27 Bacterium
28 Endosymbiont
29 Endosymbiont
30 Endosymbiont
31 Endosymbiont
32 Endosymbiont
33 Endosymbiont
34 Endosymbiont
35 Endosymbiont
36 Endosymbiont
37 Endosymbiont
38 Endosymbiont
39 Bioenergetic organelle
40 Bioenergetic organelle Allen JF (1993) Control of Gene Expression by Redox Potential and the Requirement for Chloroplast and Mitochondrial Genomes. Journal of Theoretical Biology 165:
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42 Bacterium
43 Redox regulation Bacterium
44 Host cell Redox regulation Bacterium
45 Cytosol Redox regulation Mitochondrial matrix
46 CoRR Co-Location (of gene and gene product) for Redox Regulation
47 CoRR Co-Location (of gene and gene product) for Redox Regulation Predictions of the CoRR hypothesis include:
48 CoRR Co-Location (of gene and gene product) for Redox Regulation Predictions of the CoRR hypothesis include: 1. Redox regulatory control of mitochondrial and chloroplast gene expression
49 CoRR Co-Location (of gene and gene product) for Redox Regulation Predictions of the CoRR hypothesis include: 1. Redox regulatory control of mitochondrial and chloroplast gene expression 2. When mitochondria and chloroplasts lose their function in energy conversion, they also lose their genomes
50 CoRR Co-Location (of gene and gene product) for Redox Regulation Predictions of the CoRR hypothesis include: 1. Redox regulatory control of mitochondrial and chloroplast gene expression 2. When mitochondria and chloroplasts lose their function in energy conversion, they also lose their genomes 3. Bacterial redox signalling components persist in chloroplasts and mitochondria
51 CoRR Co-Location (of gene and gene product) for Redox Regulation Predictions of the CoRR hypothesis include: 1. Redox regulatory control of mitochondrial and chloroplast gene expression 2. When mitochondria and chloroplasts lose their function in energy conversion, they also lose their genomes 3. Bacterial redox signalling components persist in chloroplasts and mitochondria 4...
52 CoRR Co-Location (of gene and gene product) for Redox Regulation Predictions of the CoRR hypothesis include: 1. Redox regulatory control of mitochondrial and chloroplast gene expression 2. When mitochondria and chloroplasts lose their function in energy conversion, they also lose their genomes 3. Bacterial redox signalling components persist in chloroplasts and mitochondria
53 Co-location for Redox Regulation - CoRR Prediction Experimental results Redox regulatory control of mitochondrial and chloroplast gene expression
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63 + ferricyanide pyruvate, malate control + ascorbate + dithiothreitol + dithionite + duroquinol + rotenone, malonate.,dicumarol + cyanide, SHAM Allen, C. A. et al Redox Report 1, S-methionine labelling of newly synthesised proteins in pea leaf mitochondria
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67 Dark (D) Light (L) D + ferricyanide D + ascorbate D + dithiothreitol D + dithionite L + DCMU D, anaerobic L + DBMIB D + duroquinol Allen, C. A. et al Redox Report 1, S-methionine labelling of newly synthesised proteins in pea leaf thylakoids
68 Dark (D) Light (L) D + ferricyanide D + ascorbate D + dithiothreitol D + dithionite L + DCMU D, anaerobic L + DBMIB D + duroquinol Allen, C. A. et al Redox Report 1, S-methionine labelling of newly synthesised proteins in pea leaf chloroplast stroma
69 Co-location for Redox Regulation - CoRR Prediction Experimental results Redox regulatory control of chloroplast and mitochondrial transcription
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72 Light 1
73 Light 1 Light 2
74 Light 1 Light 2
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76 Co-location for Redox Regulation - CoRR Prediction Experimental results Persistence of bacterial redox signalling components in chloroplasts and mitochondria
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78 CSK Chloroplast Sensor Kinase A Histidine sensor kinase homologous with Hik2 of cyanobacteria A Redox Sensor Sujith Puthiyaveetil
79 Fig. 1 A B Puthiyaveetil S, Kavanagh TA, Cain P, Sullivan JA, Newell CA, Gray JC, Robinson C, van der Giezen M, Rogers MB, Allen JF (2008) The ancestral symbiont sensor kinase CSK links photosynthesis with gene expression in chloroplasts. Proceedings of the National Academy of Sciences of the United States of America 105:
80 Puthiyaveetil S, Kavanagh TA, Cain P, Sullivan JA, Newell CA, Gray JC, Robinson C, van der Giezen M, Rogers MB, Allen JF (2008) The ancestral symbiont sensor kinase CSK links photosynthesis with gene expression in chloroplasts. Proceedings of the National Academy of Sciences of the United States of America 105:
81 Puthiyaveetil S, Kavanagh TA, Cain P, Sullivan JA, Newell CA, Gray JC, Robinson C, van der Giezen M, Rogers MB, Allen JF (2008) The ancestral symbiont sensor kinase CSK links photosynthesis with gene expression in chloroplasts. Proceedings of the National Academy of Sciences of the United States of America 105:
82 Puthiyaveetil S, Kavanagh TA, Cain P, Sullivan JA, Newell CA, Gray JC, Robinson C, van der Giezen M, Rogers MB, Allen JF (2008) The ancestral symbiont sensor kinase CSK links photosynthesis with gene expression in chloroplasts. Proceedings of the National Academy of Sciences of the United States of America 105:
83 Puthiyaveetil S, Kavanagh TA, Cain P, Sullivan JA, Newell CA, Gray JC, Robinson C, van der Giezen M, Rogers MB, Allen JF (2008) The ancestral symbiont sensor kinase CSK links photosynthesis with gene expression in chloroplasts. Proceedings of the National Academy of Sciences of the United States of America 105:
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85 Light 2 hv Light 1 hv PQ/ e- e- PQH 2 e- e- H 2 O P 680 Cyt b 6 f P 700 NADP + Photosystem II Photosystem I Redox Sensor Kinase biosynthesis biosynthesis transcription Redox Response Regulator transcription psb genes psa genes Puthiyaveetil S and Allen JF (2008) Transients in chloroplast gene transcription Biochemical and Biophysical Research Communications. 368:
86 Light 2 hv Light 1 hv PQ/ e- e- PQH 2 e- e- H 2 O P 680 Cyt b 6 f P 700 NADP + Photosystem II Photosystem I CSK Redox Sensor Kinase biosynthesis biosynthesis transcription Redox Response Regulator transcription psb genes psa genes Puthiyaveetil S and Allen JF (2008) Transients in chloroplast gene transcription Biochemical and Biophysical Research Communications. 368:
87 Puthiyaveetil S and Allen JF (2009) Chloroplast two-component systems: evolution of the link between photosynthesis and gene expression Proceedings of the Royal Society B-Biological Sciences. In press
88 The costs of DNA in mitochondria
89 The mitochondrial theory of ageing ( aging - U.S.)
90 The mitochondrial theory of ageing
91 The mitochondrial theory of ageing Errors in electron transfer - transfers to the wrong electron acceptor - occur at fixed frequency.
92 The mitochondrial theory of ageing Errors in electron transfer - transfers to the wrong electron acceptor - occur at fixed frequency. The products of these reactions damage mitochondrial genes, which then produce defective proteins, which then make more "errors" in electron transfer...damaging more genes, making more defective proteins...and so on.
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96 Even without the Mitochondrial Theory of Ageing.
97 Even without the Mitochondrial Theory of Ageing. The mitochondrion is the worst imaginable place in the cell to keep genes.
98 Even without the Mitochondrial Theory of Ageing. The mitochondrion is the worst imaginable place in the cell to keep genes. Whatever the reason for the persistence of mitochondrial genomes, it had better be a good one.
99 Separate sexes as mitochondrial division of labour
100 Why there are two sexes
101 Why there are two sexes Problem: Mitochondrial Ageing predicts that offspring should inherit their mothersʼ acquired state of accumulated damage, but they evidently do not. Babies are not born at the physical age of their mothers.
102 Why there are two sexes Problem: Mitochondrial Ageing predicts that offspring should inherit their mothersʼ acquired state of accumulated damage, but they evidently do not. Babies are not born at the physical age of their mothers. How can this be?
103 Why there are two sexes Problem: Mitochondrial Ageing predicts that offspring should inherit their mothersʼ acquired state of accumulated damage, but they evidently do not. Babies are not born at the physical age of their mothers. How can this be? Proposed solution (hypothesis): Separation of two sexes allows specialisation of mitochondria either as genetic templates (female germ line) or as energy-converters (male germ line).
104 Why there are two sexes Problem: Mitochondrial Ageing predicts that offspring should inherit their mothersʼ acquired state of accumulated damage, but they evidently do not. Babies are not born at the physical age of their mothers. How can this be? Proposed solution (hypothesis): Separation of two sexes allows specialisation of mitochondria either as genetic templates (female germ line) or as energy-converters (male germ line). And they can never be both.
105 Oocyte Sperm Zygote + Male germ line Female germ line Female somatic line Male somatic line
106 Oocyte Sperm Zygote + Male germ line Female germ line Female somatic line Male somatic line
107 Oocyte Sperm Zygote + Male germ line Female germ line Female somatic line Male somatic line
108 Oocyte Sperm Zygote + Male germ line Female germ line Female somatic line Male somatic line
109 Oocyte Sperm Zygote + Male germ line Female germ line Female somatic line Male somatic line
110 Oocyte Sperm Zygote + + Male germ line Female germ line Female somatic line Male somatic line
111 Oocyte Sperm Zygote + + Male germ line Female germ line Female somatic line Male somatic line Allen, J F (1996) J. Theor. Biol. 180,
112 Separate sexes as mitochondrial division of labour Predictions:
113 Separate sexes as mitochondrial division of labour Predictions: Mitochondria are maternally inherited
114 Separate sexes as mitochondrial division of labour Predictions: Mitochondria are maternally inherited Oocytes (eggs) carry protected, template mitochondria, and are therefore sequestered at an early stage in female development
115 Separate sexes as mitochondrial division of labour Predictions: Mitochondria are maternally inherited Oocytes (eggs) carry protected, template mitochondria, and are therefore sequestered at an early stage in female development Females have a time-limited reproductive capacity - oocyte mitochondria become useless as genetic templates after a certain threshold of damage is reached
116 Separate sexes as mitochondrial division of labour Predictions: Mitochondria are maternally inherited Oocytes (eggs) carry protected, template mitochondria, and are therefore sequestered at an early stage in female development Females have a time-limited reproductive capacity - oocyte mitochondria become useless as genetic templates after a certain threshold of damage is reached Somatic, reproductive cloning will produce elderly offspring if somatic mitochondria are introduced into the oocyte. Dolly: 6+5=11
117 Separate sexes as mitochondrial division of labour Predictions: Mitochondria are maternally inherited Oocytes (eggs) carry protected, template mitochondria, and are therefore sequestered at an early stage in female development Females have a time-limited reproductive capacity - oocyte mitochondria become useless as genetic templates after a certain threshold of damage is reached Somatic, reproductive cloning will produce elderly offspring if somatic mitochondria are introduced into the oocyte. Dolly: 6+5=11 An immortal line of genetically repressed mitochondria in the female germ line; from egg back to egg
118 Summary
119 Summary Mitochondria and chloroplasts:
120 Summary Mitochondria and chloroplasts: evolved from bacteria
121 Summary Mitochondria and chloroplasts: evolved from bacteria are (photo)chemical fuel cells that provide all our energy
122 Summary Mitochondria and chloroplasts: evolved from bacteria are (photo)chemical fuel cells that provide all our energy retain their own genes and genomes in order to do so
123 Summary Mitochondria and chloroplasts: evolved from bacteria are (photo)chemical fuel cells that provide all our energy retain their own genes and genomes in order to do so mostly destroy themselves (and, eventually, us) in consequence
124 Summary Mitochondria and chloroplasts: evolved from bacteria are (photo)chemical fuel cells that provide all our energy retain their own genes and genomes in order to do so mostly destroy themselves (and, eventually, us) in consequence but are predicted to exist also in female germ lines as protected genetic templates, incapable of energy conversion, and from which all other mitochondria and chloroplasts derive
125 Coda. Two views of mitochondria View 1
126 Coda. Two views of mitochondria View 1 John Burn (Newcastle Institute of Clinical Genetics). Quoted in The Times, 9th September 2005
127 Coda. Two views of mitochondria View 1 John Burn (Newcastle Institute of Clinical Genetics). Quoted in The Times, 9th September 2005 Mitochondria:
128 Coda. Two views of mitochondria View 1 John Burn (Newcastle Institute of Clinical Genetics). Quoted in The Times, 9th September 2005 Mitochondria: are not part of the genetic material that we consider makes us as human beings.
129 Coda. Two views of mitochondria View 1 John Burn (Newcastle Institute of Clinical Genetics). Quoted in The Times, 9th September 2005 Mitochondria: are not part of the genetic material that we consider makes us as human beings. My belief is that what we are doing is changing a battery that doesnʼt work for one that does.changing the mitochondria wonʼt affect the important DNA.
130 Coda. Two views of mitochondria View 2
131 Coda. Two views of mitochondria View 2 Nick Lane. Power, Sex, Suicide. Mitochondria and the Meaning of Life. Oxford University Press
132 Coda. Two views of mitochondria View 2 Nick Lane. Power, Sex, Suicide. Mitochondria and the Meaning of Life. Oxford University Press Mitochondria:
133 Coda. Two views of mitochondria View 2 Nick Lane. Power, Sex, Suicide. Mitochondria and the Meaning of Life. Oxford University Press Mitochondria: give striking new insights into why we are here at all, whether we are alone in the universe, why we have our sense of individuality, why we should make love, where we trace our ancestral roots, why we must age and die in short, into the meaning of life.
134 a chloroplast Christmas-Rose leaf SEM cross-section; Science Photo Library (SPL)
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136 halfont & Latimer rleywood ckmansworth p p s h p d erivale on ss Ruislip B Rayners Lane Northolt Ealing Broadway Sudbury Town Hanger Lane 3 Ealing Common Northfields South Ealing Hounslow Central Croxley A Moor Park Northwood Northwood Hills Ruislip Manor Alperton Park Royal North Ealing Eastcote Watford Acton Town on Manor Chiswick slow Park East Osterley nd symbols oo al t ondon ersmith & City Pinner West Harrow South Harrow Sudbury Hill Under construction West Acton South Acton Turnham Green North Harrow North Acton Gunnersbury Kew Gardens Richmond Harrow & Wealdstone Northwick Park South Kenton North Wembley Wembley Central Stonebridge Park Harlesden Willesden Junction Maida Vale Kilburn Park Warwick Avenue Paddington Royal Oak Westbourne Park Paddington Ladbroke Grove Latimer Road East Acton 2 Acton Central Shepherd's Bush Goldhawk Road Hammersmith Stamford Ravenscourt Brook Park Northern Piccadilly Victoria Waterloo & City restricted service - see opposite key Docklands Light Railway National Rail White City Kenton Preston Road Wembley Park Neasden Dollis Hill Kensal Rise Brondesbury Kensal Green Queen's Park Shepherd's Bush Barons Court Holland Park Kensington (Olympia) West Kensington West Brompton Fulham Broadway Parsons Green Putney Bridge East Putney Southfields Wimbledon Park Wimbledon Stanmore Canons Park Queensbury Kingsbury Brondesbury Park Interchange stations Earl's Court Notting Hill Gate River Thames Connections with National Rail Willesden Green Edgware Road Bayswater Gloucester Road Connections with riverboat services Airport interchange Connection with Tramlink Closed Sundays Edgware Kilburn Edgware Road West Hampstead 1 South Kensington Burnt Oak Finchley Road Lancaster Bond Queensway Gate Street Knightsbridge Colindale Hendon Central Marylebone Marble Arch High Street Hyde Park Kensington Corner Swiss Cottage St. John's Wood Sloane Square Colliers Wood Brent Cross Finchley Road & Frognal Victoria Pimlico Tooting Bec Golders Green 200m Vauxhall Baker Street Oxford Circus Green Park St. James's Park Clapham South Hampstead Piccadilly Circus Westminster Stockwell Clapham North Clapham High Street 100m Balham Belsize Park 2 Great Portland Street Tooting Broadway Tottenham Court Road Waterloo Clapham Common Hampstead Heath Chalk Farm Camden Town Mornington Crescent Warren Street Regent's Park Euston Oval Mill Hill East Euston Square Goodge Street Holborn Mansion House Embankment Temple Southwark Waterloo East 2 Blackfriars Farringdon Barbican Moorgate St. Paul's Chancery Lane Bank Covent Garden Cannon Street Leicester Square Kennington Gospel Oak Kentish Town West Euston 200m Charing Cross Charing Cross 100m Lambeth North Brixton Camden Road King's Cross St. Pancras Russell Square Totteridge & Whetstone Woodside Park West Finchley Finchley Central East Finchley Highgate Archway Tufnell Park Kentish Town Elephant & Castle 100m 100m Holloway Road Caledonian Road Angel Borough Bounds Green Turnpike Lane Manor House Arsenal Arnos Grove Wood Green Caledonian Road & Barnsbury Old Street Oakwood Southgate Highbury & Islington 1 Aldgate Finsbury Park Canonbury Monument Tower Hill Fenchurch Street 150m Tower Gateway River Thames London Bridge Explanation of zones D C B A Station in Zone D Station in Zone C Station in Zone B Station in Zone A Station in Zone 6 and Zone A Station in Zone 6 Station in Zone 5 Station in Zone 4 Station in both zones Station in Zone 3 Station in Zone 2 Liverpool Street Bermondsey New Cross Gate Seven Sisters Dalston Kingsland Aldgate East Rotherhithe Canada Water Surrey Quays Bakerloo Central Circle District District East London Tottenham Hale Hackney Central Bethnal Green Shoreditch Blackhorse Road Homerton 2 Whitechapel Shadwell Walthamstow Central Hackney Wick Mile End 2 Stepney Green Wapping Limehouse New Cross 2 Bow Road All Saints Westferry West India Quay Canary Wharf Heron Quays South Quay Crossharbour & London Arena Lewisham Mudchute Island Gardens 3 Elverson Road Buckhurst Hill South Woodford Snaresbrook Leytonstone Stratford Bow Church 200m Devons Road Poplar Deptford Bridge Woodford Leyton Loughton Pudding Mill Lane Harrowon-the-Hill Bromleyby-Bow Cutty Sark for Maritime Greenwich Greenwich Blackwall Special fares apply for single and return tickets to and from Harrow & Wealdstone. No service Woodford - Hainault after 2000 daily. Cannon Street open until 2100 Mondays to Fridays. Closed Saturdays and Sundays. Earl s Court - Kensington (Olympia) 0700 to 2345 Mondays to Saturdays, 0800 to 2345 Sundays. Shoreditch - Whitechapel open 0700 to 1000 and 1530 to 1900 Mondays to Fridays. East India Roding Valley 4 Debden Upton Par Plaistow West Ham 3 West Silvertown 3 Eppin Theydon Chigwell Grange Hill Newbury Park Redbridge Wanstead North Greenwich Points to remember Hammersmith & City Metropolitan Northern Piccadilly Gants Hill Upney Ba East Ha Bus to London City Airpor Canning Town Roy Under construction Pontoon Doc Silverto North W No service W late evening For Chesham on most train On Sundays b Camden Tow No entry to C between 130 Heathrow Te Mondays to S No service U 0615 to
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139 1 Rudi Lemberg
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141 Ebikabowei Bozimo Carol A. Allen Iskander Ibrahim John F. Allen Azma Shiyam Thomas Buckland Sujith Puthiyaveetil
142 Ebikabowei Bozimo Carol A. Allen Iskander Ibrahim John F. Allen Azma Shiyam Thomas Buckland Sujith Puthiyaveetil The end. Thank you for listening.
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