Oxygen-binding proteins aid oxygen diffusion to enhance fitness of a yeast model of multicellularity.
Oxygen availability is a key factor in the evolution of multicellularity, as larger and more sophisticated organisms often require mechanisms allowing efficient oxygen delivery to their tissues. One such mechanism is the presence of oxygen-binding proteins, such as globins and hemerythrins, which ar...
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| Format: | Article |
| Language: | English |
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Public Library of Science (PLoS)
2025-01-01
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| Series: | PLoS Biology |
| Online Access: | https://doi.org/10.1371/journal.pbio.3002975 |
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| author | Whitney Wong Pablo Bravo Peter J Yunker William C Ratcliff Anthony J Burnetti |
| author_facet | Whitney Wong Pablo Bravo Peter J Yunker William C Ratcliff Anthony J Burnetti |
| author_sort | Whitney Wong |
| collection | DOAJ |
| description | Oxygen availability is a key factor in the evolution of multicellularity, as larger and more sophisticated organisms often require mechanisms allowing efficient oxygen delivery to their tissues. One such mechanism is the presence of oxygen-binding proteins, such as globins and hemerythrins, which arose in the ancestor of bilaterian animals. Despite their importance, the precise mechanisms by which oxygen-binding proteins influenced the early stages of multicellular evolution under varying environmental oxygen levels are not yet clear. We address this knowledge gap by heterologously expressing the oxygen-binding proteins myoglobin and myohemerythrin in snowflake yeast, a model system of simple, undifferentiated multicellularity. These proteins increased the depth and rate of oxygen diffusion, increasing the fitness of snowflake yeast growing aerobically. Experiments show that, paradoxically, oxygen-binding proteins confer a greater fitness benefit for larger organisms when O2 is least limiting. We show via biophysical modeling that this is because facilitated diffusion is more efficient when oxygen is abundant, transporting a greater quantity of O2 which can be used for metabolism. By alleviating anatomical diffusion limitations to oxygen consumption, the evolution of oxygen-binding proteins in the oxygen-rich Neoproterozoic may have been a key breakthrough enabling the evolution of increasingly large, complex multicellular metazoan lineages. |
| format | Article |
| id | doaj-art-47bf26e06130462bb37fa3828f2ca599 |
| institution | Kabale University |
| issn | 1544-9173 1545-7885 |
| language | English |
| publishDate | 2025-01-01 |
| publisher | Public Library of Science (PLoS) |
| record_format | Article |
| series | PLoS Biology |
| spelling | doaj-art-47bf26e06130462bb37fa3828f2ca5992025-02-07T05:30:16ZengPublic Library of Science (PLoS)PLoS Biology1544-91731545-78852025-01-01231e300297510.1371/journal.pbio.3002975Oxygen-binding proteins aid oxygen diffusion to enhance fitness of a yeast model of multicellularity.Whitney WongPablo BravoPeter J YunkerWilliam C RatcliffAnthony J BurnettiOxygen availability is a key factor in the evolution of multicellularity, as larger and more sophisticated organisms often require mechanisms allowing efficient oxygen delivery to their tissues. One such mechanism is the presence of oxygen-binding proteins, such as globins and hemerythrins, which arose in the ancestor of bilaterian animals. Despite their importance, the precise mechanisms by which oxygen-binding proteins influenced the early stages of multicellular evolution under varying environmental oxygen levels are not yet clear. We address this knowledge gap by heterologously expressing the oxygen-binding proteins myoglobin and myohemerythrin in snowflake yeast, a model system of simple, undifferentiated multicellularity. These proteins increased the depth and rate of oxygen diffusion, increasing the fitness of snowflake yeast growing aerobically. Experiments show that, paradoxically, oxygen-binding proteins confer a greater fitness benefit for larger organisms when O2 is least limiting. We show via biophysical modeling that this is because facilitated diffusion is more efficient when oxygen is abundant, transporting a greater quantity of O2 which can be used for metabolism. By alleviating anatomical diffusion limitations to oxygen consumption, the evolution of oxygen-binding proteins in the oxygen-rich Neoproterozoic may have been a key breakthrough enabling the evolution of increasingly large, complex multicellular metazoan lineages.https://doi.org/10.1371/journal.pbio.3002975 |
| spellingShingle | Whitney Wong Pablo Bravo Peter J Yunker William C Ratcliff Anthony J Burnetti Oxygen-binding proteins aid oxygen diffusion to enhance fitness of a yeast model of multicellularity. PLoS Biology |
| title | Oxygen-binding proteins aid oxygen diffusion to enhance fitness of a yeast model of multicellularity. |
| title_full | Oxygen-binding proteins aid oxygen diffusion to enhance fitness of a yeast model of multicellularity. |
| title_fullStr | Oxygen-binding proteins aid oxygen diffusion to enhance fitness of a yeast model of multicellularity. |
| title_full_unstemmed | Oxygen-binding proteins aid oxygen diffusion to enhance fitness of a yeast model of multicellularity. |
| title_short | Oxygen-binding proteins aid oxygen diffusion to enhance fitness of a yeast model of multicellularity. |
| title_sort | oxygen binding proteins aid oxygen diffusion to enhance fitness of a yeast model of multicellularity |
| url | https://doi.org/10.1371/journal.pbio.3002975 |
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