Heterologous expression of genes from a cyanobacterial endosymbiont highlights substrate exchanges with its diatom host
A few genera of diatoms are widespread and thrive in low-nutrient waters of the open ocean due to their close association with N(2)-fixing, filamentous heterocyst-forming cyanobacteria. In one of these symbioses, the symbiont, Richelia euintracellularis, has penetrated the cell envelope of the host,...
Published in: | PNAS Nexus |
---|---|
Main Authors: | , , , , , |
Format: | Text |
Language: | English |
Published: |
Oxford University Press
2023
|
Subjects: | |
Online Access: | http://www.ncbi.nlm.nih.gov/pmc/articles/PMC10299089/ http://www.ncbi.nlm.nih.gov/pubmed/37383020 https://doi.org/10.1093/pnasnexus/pgad194 |
id |
ftpubmed:oai:pubmedcentral.nih.gov:10299089 |
---|---|
record_format |
openpolar |
spelling |
ftpubmed:oai:pubmedcentral.nih.gov:10299089 2023-07-23T04:20:44+02:00 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 2023-06-27 http://www.ncbi.nlm.nih.gov/pmc/articles/PMC10299089/ http://www.ncbi.nlm.nih.gov/pubmed/37383020 https://doi.org/10.1093/pnasnexus/pgad194 en eng Oxford University Press http://www.ncbi.nlm.nih.gov/pmc/articles/PMC10299089/ http://www.ncbi.nlm.nih.gov/pubmed/37383020 http://dx.doi.org/10.1093/pnasnexus/pgad194 © The Author(s) 2023. Published by Oxford University Press on behalf of National Academy of Sciences. https://creativecommons.org/licenses/by/4.0/This is an Open Access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited. PNAS Nexus Biological Health and Medical Sciences Text 2023 ftpubmed https://doi.org/10.1093/pnasnexus/pgad194 2023-07-02T01:08:20Z A few genera of diatoms are widespread and thrive in low-nutrient waters of the open ocean due to their close association with N(2)-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 N(2) 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 N(2) fixation. This knowledge is key to understanding the physiology of the globally significant H. hauckii–R. euintracellularis symbiosis. Text North Atlantic PubMed Central (PMC) PNAS Nexus 2 6 |
institution |
Open Polar |
collection |
PubMed Central (PMC) |
op_collection_id |
ftpubmed |
language |
English |
topic |
Biological Health and Medical Sciences |
spellingShingle |
Biological Health and Medical Sciences 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 |
topic_facet |
Biological Health and Medical Sciences |
description |
A few genera of diatoms are widespread and thrive in low-nutrient waters of the open ocean due to their close association with N(2)-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 N(2) 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 N(2) fixation. This knowledge is key to understanding the physiology of the globally significant H. hauckii–R. euintracellularis symbiosis. |
format |
Text |
author |
Nieves-Morión, Mercedes Camargo, Sergio Bardi, Sepehr Ruiz, María Teresa Flores, Enrique Foster, Rachel A |
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 |
publishDate |
2023 |
url |
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC10299089/ http://www.ncbi.nlm.nih.gov/pubmed/37383020 https://doi.org/10.1093/pnasnexus/pgad194 |
genre |
North Atlantic |
genre_facet |
North Atlantic |
op_source |
PNAS Nexus |
op_relation |
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC10299089/ http://www.ncbi.nlm.nih.gov/pubmed/37383020 http://dx.doi.org/10.1093/pnasnexus/pgad194 |
op_rights |
© The Author(s) 2023. Published by Oxford University Press on behalf of National Academy of Sciences. https://creativecommons.org/licenses/by/4.0/This is an Open Access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited. |
op_doi |
https://doi.org/10.1093/pnasnexus/pgad194 |
container_title |
PNAS Nexus |
container_volume |
2 |
container_issue |
6 |
_version_ |
1772185420455477248 |