Heterologous expression of genes from a cyanobacterial endosymbiont highlights substrate exchanges with its diatom host
Abstract A few genera of diatoms are widespread and thrive in low-nutrient waters of the open ocean due to their close association with N2-fixing, filamentous heterocyst-forming cyanobacteria. In one of these symbioses, the symbiont, Richelia euintracellularis, has penetrated the cell envelope of th...
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2023
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Online Access: | http://dx.doi.org/10.1093/pnasnexus/pgad194 https://academic.oup.com/pnasnexus/article-pdf/2/6/pgad194/51011879/pgad194.pdf |
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croxfordunivpr:10.1093/pnasnexus/pgad194 2024-09-15T18:23:49+00:00 Heterologous expression of genes from a cyanobacterial endosymbiont highlights substrate exchanges with its diatom host Nieves-Morión, Mercedes Camargo, Sergio Bardi, Sepehr Ruiz, María Teresa Flores, Enrique Foster, Rachel A Bayer, Edward The Swedish Research Council Knut and Alice Wallenberg Foundation 2023 http://dx.doi.org/10.1093/pnasnexus/pgad194 https://academic.oup.com/pnasnexus/article-pdf/2/6/pgad194/51011879/pgad194.pdf en eng Oxford University Press (OUP) https://creativecommons.org/licenses/by/4.0/ PNAS Nexus volume 2, issue 6 ISSN 2752-6542 journal-article 2023 croxfordunivpr https://doi.org/10.1093/pnasnexus/pgad194 2024-08-19T04:23:19Z Abstract A few genera of diatoms are widespread and thrive in low-nutrient waters of the open ocean due to their close association with N2-fixing, filamentous heterocyst-forming cyanobacteria. In one of these symbioses, the symbiont, Richelia euintracellularis, has penetrated the cell envelope of the host, Hemiaulus hauckii, and lives inside the host cytoplasm. How the partners interact, including how the symbiont sustains high rates of N2 fixation, is unstudied. Since R. euintracellularis has evaded isolation, heterologous expression of genes in model laboratory organisms was performed to identify the function of proteins from the endosymbiont. Gene complementation of a cyanobacterial invertase mutant and expression of the protein in Escherichia coli showed that R. euintracellularis HH01 possesses a neutral invertase that splits sucrose producing glucose and fructose. Several solute-binding proteins (SBPs) of ABC transporters encoded in the genome of R. euintracellularis HH01 were expressed in E. coli, and their substrates were characterized. The selected SBPs directly linked the host as the source of several substrates, e.g. sugars (sucrose and galactose), amino acids (glutamate and phenylalanine), and a polyamine (spermidine), to support the cyanobacterial symbiont. Finally, transcripts of genes encoding the invertase and SBPs were consistently detected in wild populations of H. hauckii collected from multiple stations and depths in the western tropical North Atlantic. Our results support the idea that the diatom host provides the endosymbiotic cyanobacterium with organic carbon to fuel N2 fixation. This knowledge is key to understanding the physiology of the globally significant H. hauckii–R. euintracellularis symbiosis. Article in Journal/Newspaper North Atlantic Oxford University Press PNAS Nexus 2 6 |
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Open Polar |
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Oxford University Press |
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croxfordunivpr |
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English |
description |
Abstract A few genera of diatoms are widespread and thrive in low-nutrient waters of the open ocean due to their close association with N2-fixing, filamentous heterocyst-forming cyanobacteria. In one of these symbioses, the symbiont, Richelia euintracellularis, has penetrated the cell envelope of the host, Hemiaulus hauckii, and lives inside the host cytoplasm. How the partners interact, including how the symbiont sustains high rates of N2 fixation, is unstudied. Since R. euintracellularis has evaded isolation, heterologous expression of genes in model laboratory organisms was performed to identify the function of proteins from the endosymbiont. Gene complementation of a cyanobacterial invertase mutant and expression of the protein in Escherichia coli showed that R. euintracellularis HH01 possesses a neutral invertase that splits sucrose producing glucose and fructose. Several solute-binding proteins (SBPs) of ABC transporters encoded in the genome of R. euintracellularis HH01 were expressed in E. coli, and their substrates were characterized. The selected SBPs directly linked the host as the source of several substrates, e.g. sugars (sucrose and galactose), amino acids (glutamate and phenylalanine), and a polyamine (spermidine), to support the cyanobacterial symbiont. Finally, transcripts of genes encoding the invertase and SBPs were consistently detected in wild populations of H. hauckii collected from multiple stations and depths in the western tropical North Atlantic. Our results support the idea that the diatom host provides the endosymbiotic cyanobacterium with organic carbon to fuel N2 fixation. This knowledge is key to understanding the physiology of the globally significant H. hauckii–R. euintracellularis symbiosis. |
author2 |
Bayer, Edward The Swedish Research Council Knut and Alice Wallenberg Foundation |
format |
Article in Journal/Newspaper |
author |
Nieves-Morión, Mercedes Camargo, Sergio Bardi, Sepehr Ruiz, María Teresa Flores, Enrique Foster, Rachel A |
spellingShingle |
Nieves-Morión, Mercedes Camargo, Sergio Bardi, Sepehr Ruiz, María Teresa Flores, Enrique Foster, Rachel A Heterologous expression of genes from a cyanobacterial endosymbiont highlights substrate exchanges with its diatom host |
author_facet |
Nieves-Morión, Mercedes Camargo, Sergio Bardi, Sepehr Ruiz, María Teresa Flores, Enrique Foster, Rachel A |
author_sort |
Nieves-Morión, Mercedes |
title |
Heterologous expression of genes from a cyanobacterial endosymbiont highlights substrate exchanges with its diatom host |
title_short |
Heterologous expression of genes from a cyanobacterial endosymbiont highlights substrate exchanges with its diatom host |
title_full |
Heterologous expression of genes from a cyanobacterial endosymbiont highlights substrate exchanges with its diatom host |
title_fullStr |
Heterologous expression of genes from a cyanobacterial endosymbiont highlights substrate exchanges with its diatom host |
title_full_unstemmed |
Heterologous expression of genes from a cyanobacterial endosymbiont highlights substrate exchanges with its diatom host |
title_sort |
heterologous expression of genes from a cyanobacterial endosymbiont highlights substrate exchanges with its diatom host |
publisher |
Oxford University Press (OUP) |
publishDate |
2023 |
url |
http://dx.doi.org/10.1093/pnasnexus/pgad194 https://academic.oup.com/pnasnexus/article-pdf/2/6/pgad194/51011879/pgad194.pdf |
genre |
North Atlantic |
genre_facet |
North Atlantic |
op_source |
PNAS Nexus volume 2, issue 6 ISSN 2752-6542 |
op_rights |
https://creativecommons.org/licenses/by/4.0/ |
op_doi |
https://doi.org/10.1093/pnasnexus/pgad194 |
container_title |
PNAS Nexus |
container_volume |
2 |
container_issue |
6 |
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1810464078044332032 |