The Transcriptional Cycle Is Suited to Daytime N<sub>2</sub> Fixation in the Unicellular Cyanobacterium “<italic toggle="yes">Candidatus</italic> Atelocyanobacterium thalassa” (UCYN-A)

ABSTRACT Symbiosis between a marine alga and a N2-fixing cyanobacterium (Cyanobacterium UCYN-A) is geographically widespread in the oceans and is important in the marine N cycle. UCYN-A is uncultivated and is an unusual unicellular cyanobacterium because it lacks many metabolic functions, including...

Descripción completa

Guardado en:

Detalles Bibliográficos
Autores principales:	María del Carmen Muñoz-Marín, Irina N. Shilova, Tuo Shi, Hanna Farnelid, Ana María Cabello, Jonathan P. Zehr
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2019
Materias:	cyanobacteria diel cycle marine microbiology nitrogen fixation symbiosis whole-genome expression Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/d6c22c9256f94ce593caae922fa057db
Etiquetas:	Agregar Etiqueta Sin Etiquetas, Sea el primero en etiquetar este registro!

id	oai:doaj.org-article:d6c22c9256f94ce593caae922fa057db
record_format	dspace
spelling	oai:doaj.org-article:d6c22c9256f94ce593caae922fa057db2021-11-15T15:55:14ZThe Transcriptional Cycle Is Suited to Daytime N<sub>2</sub> Fixation in the Unicellular Cyanobacterium “<italic toggle="yes">Candidatus</italic> Atelocyanobacterium thalassa” (UCYN-A)10.1128/mBio.02495-182150-7511https://doaj.org/article/d6c22c9256f94ce593caae922fa057db2019-02-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.02495-18https://doaj.org/toc/2150-7511ABSTRACT Symbiosis between a marine alga and a N2-fixing cyanobacterium (Cyanobacterium UCYN-A) is geographically widespread in the oceans and is important in the marine N cycle. UCYN-A is uncultivated and is an unusual unicellular cyanobacterium because it lacks many metabolic functions, including oxygenic photosynthesis and carbon fixation, which are typical in cyanobacteria. It is now presumed to be an obligate symbiont of haptophytes closely related to Braarudosphaera bigelowii. N2-fixing cyanobacteria use different strategies to avoid inhibition of N2 fixation by the oxygen evolved in photosynthesis. Most unicellular cyanobacteria temporally separate the two incompatible activities by fixing N2 only at night, but, surprisingly, UCYN-A appears to fix N2 during the day. The goal of this study was to determine how the unicellular UCYN-A strain coordinates N2 fixation and general metabolism compared to other marine cyanobacteria. We found that UCYN-A has distinct daily cycles of many genes despite the fact that it lacks two of the three circadian clock genes found in most cyanobacteria. We also found that the transcription patterns in UCYN-A are more similar to those in marine cyanobacteria that are capable of aerobic N2 fixation in the light, such as Trichodesmium and heterocyst-forming cyanobacteria, than to those in Crocosphaera or Cyanothece species, which are more closely related to unicellular marine cyanobacteria evolutionarily. Our findings suggest that the symbiotic interaction has resulted in a shift of transcriptional regulation to coordinate UCYN-A metabolism with that of the phototrophic eukaryotic host, thus allowing efficient coupling of N2 fixation (by the cyanobacterium) to the energy obtained from photosynthesis (by the eukaryotic unicellular alga) in the light. IMPORTANCE The symbiotic N2-fixing cyanobacterium UCYN-A, which is closely related to Braarudosphaera bigelowii, and its eukaryotic algal host have been shown to be globally distributed and important in open-ocean N2 fixation. These unique cyanobacteria have reduced metabolic capabilities, even lacking genes for oxygenic photosynthesis and carbon fixation. Cyanobacteria generally use energy from photosynthesis for nitrogen fixation but require mechanisms for avoiding inactivation of the oxygen-sensitive nitrogenase enzyme by ambient oxygen (O2) or the O2 evolved through photosynthesis. This study showed that symbiosis between the N2-fixing cyanobacterium UCYN-A and its eukaryotic algal host has led to adaptation of its daily gene expression pattern in order to enable daytime aerobic N2 fixation, which is likely more energetically efficient than fixing N2 at night, as found in other unicellular marine cyanobacteria.María del Carmen Muñoz-MarínIrina N. ShilovaTuo ShiHanna FarnelidAna María CabelloJonathan P. ZehrAmerican Society for Microbiologyarticlecyanobacteriadiel cyclemarine microbiologynitrogen fixationsymbiosiswhole-genome expressionMicrobiologyQR1-502ENmBio, Vol 10, Iss 1 (2019)
institution	DOAJ
collection	DOAJ
language	EN
topic	cyanobacteria diel cycle marine microbiology nitrogen fixation symbiosis whole-genome expression Microbiology QR1-502
spellingShingle	cyanobacteria diel cycle marine microbiology nitrogen fixation symbiosis whole-genome expression Microbiology QR1-502 María del Carmen Muñoz-Marín Irina N. Shilova Tuo Shi Hanna Farnelid Ana María Cabello Jonathan P. Zehr The Transcriptional Cycle Is Suited to Daytime N<sub>2</sub> Fixation in the Unicellular Cyanobacterium “<italic toggle="yes">Candidatus</italic> Atelocyanobacterium thalassa” (UCYN-A)
description	ABSTRACT Symbiosis between a marine alga and a N2-fixing cyanobacterium (Cyanobacterium UCYN-A) is geographically widespread in the oceans and is important in the marine N cycle. UCYN-A is uncultivated and is an unusual unicellular cyanobacterium because it lacks many metabolic functions, including oxygenic photosynthesis and carbon fixation, which are typical in cyanobacteria. It is now presumed to be an obligate symbiont of haptophytes closely related to Braarudosphaera bigelowii. N2-fixing cyanobacteria use different strategies to avoid inhibition of N2 fixation by the oxygen evolved in photosynthesis. Most unicellular cyanobacteria temporally separate the two incompatible activities by fixing N2 only at night, but, surprisingly, UCYN-A appears to fix N2 during the day. The goal of this study was to determine how the unicellular UCYN-A strain coordinates N2 fixation and general metabolism compared to other marine cyanobacteria. We found that UCYN-A has distinct daily cycles of many genes despite the fact that it lacks two of the three circadian clock genes found in most cyanobacteria. We also found that the transcription patterns in UCYN-A are more similar to those in marine cyanobacteria that are capable of aerobic N2 fixation in the light, such as Trichodesmium and heterocyst-forming cyanobacteria, than to those in Crocosphaera or Cyanothece species, which are more closely related to unicellular marine cyanobacteria evolutionarily. Our findings suggest that the symbiotic interaction has resulted in a shift of transcriptional regulation to coordinate UCYN-A metabolism with that of the phototrophic eukaryotic host, thus allowing efficient coupling of N2 fixation (by the cyanobacterium) to the energy obtained from photosynthesis (by the eukaryotic unicellular alga) in the light. IMPORTANCE The symbiotic N2-fixing cyanobacterium UCYN-A, which is closely related to Braarudosphaera bigelowii, and its eukaryotic algal host have been shown to be globally distributed and important in open-ocean N2 fixation. These unique cyanobacteria have reduced metabolic capabilities, even lacking genes for oxygenic photosynthesis and carbon fixation. Cyanobacteria generally use energy from photosynthesis for nitrogen fixation but require mechanisms for avoiding inactivation of the oxygen-sensitive nitrogenase enzyme by ambient oxygen (O2) or the O2 evolved through photosynthesis. This study showed that symbiosis between the N2-fixing cyanobacterium UCYN-A and its eukaryotic algal host has led to adaptation of its daily gene expression pattern in order to enable daytime aerobic N2 fixation, which is likely more energetically efficient than fixing N2 at night, as found in other unicellular marine cyanobacteria.
format	article
author	María del Carmen Muñoz-Marín Irina N. Shilova Tuo Shi Hanna Farnelid Ana María Cabello Jonathan P. Zehr
author_facet	María del Carmen Muñoz-Marín Irina N. Shilova Tuo Shi Hanna Farnelid Ana María Cabello Jonathan P. Zehr
author_sort	María del Carmen Muñoz-Marín
title	The Transcriptional Cycle Is Suited to Daytime N<sub>2</sub> Fixation in the Unicellular Cyanobacterium “<italic toggle="yes">Candidatus</italic> Atelocyanobacterium thalassa” (UCYN-A)
title_short	The Transcriptional Cycle Is Suited to Daytime N<sub>2</sub> Fixation in the Unicellular Cyanobacterium “<italic toggle="yes">Candidatus</italic> Atelocyanobacterium thalassa” (UCYN-A)
title_full	The Transcriptional Cycle Is Suited to Daytime N<sub>2</sub> Fixation in the Unicellular Cyanobacterium “<italic toggle="yes">Candidatus</italic> Atelocyanobacterium thalassa” (UCYN-A)
title_fullStr	The Transcriptional Cycle Is Suited to Daytime N<sub>2</sub> Fixation in the Unicellular Cyanobacterium “<italic toggle="yes">Candidatus</italic> Atelocyanobacterium thalassa” (UCYN-A)
title_full_unstemmed	The Transcriptional Cycle Is Suited to Daytime N<sub>2</sub> Fixation in the Unicellular Cyanobacterium “<italic toggle="yes">Candidatus</italic> Atelocyanobacterium thalassa” (UCYN-A)
title_sort	transcriptional cycle is suited to daytime n<sub>2</sub> fixation in the unicellular cyanobacterium “<italic toggle="yes">candidatus</italic> atelocyanobacterium thalassa” (ucyn-a)
publisher	American Society for Microbiology
publishDate	2019
url	https://doaj.org/article/d6c22c9256f94ce593caae922fa057db
work_keys_str_mv	AT mariadelcarmenmunozmarin thetranscriptionalcycleissuitedtodaytimensub2subfixationintheunicellularcyanobacteriumitalictoggleyescandidatusitalicatelocyanobacteriumthalassaucyna AT irinanshilova thetranscriptionalcycleissuitedtodaytimensub2subfixationintheunicellularcyanobacteriumitalictoggleyescandidatusitalicatelocyanobacteriumthalassaucyna AT tuoshi thetranscriptionalcycleissuitedtodaytimensub2subfixationintheunicellularcyanobacteriumitalictoggleyescandidatusitalicatelocyanobacteriumthalassaucyna AT hannafarnelid thetranscriptionalcycleissuitedtodaytimensub2subfixationintheunicellularcyanobacteriumitalictoggleyescandidatusitalicatelocyanobacteriumthalassaucyna AT anamariacabello thetranscriptionalcycleissuitedtodaytimensub2subfixationintheunicellularcyanobacteriumitalictoggleyescandidatusitalicatelocyanobacteriumthalassaucyna AT jonathanpzehr thetranscriptionalcycleissuitedtodaytimensub2subfixationintheunicellularcyanobacteriumitalictoggleyescandidatusitalicatelocyanobacteriumthalassaucyna AT mariadelcarmenmunozmarin transcriptionalcycleissuitedtodaytimensub2subfixationintheunicellularcyanobacteriumitalictoggleyescandidatusitalicatelocyanobacteriumthalassaucyna AT irinanshilova transcriptionalcycleissuitedtodaytimensub2subfixationintheunicellularcyanobacteriumitalictoggleyescandidatusitalicatelocyanobacteriumthalassaucyna AT tuoshi transcriptionalcycleissuitedtodaytimensub2subfixationintheunicellularcyanobacteriumitalictoggleyescandidatusitalicatelocyanobacteriumthalassaucyna AT hannafarnelid transcriptionalcycleissuitedtodaytimensub2subfixationintheunicellularcyanobacteriumitalictoggleyescandidatusitalicatelocyanobacteriumthalassaucyna AT anamariacabello transcriptionalcycleissuitedtodaytimensub2subfixationintheunicellularcyanobacteriumitalictoggleyescandidatusitalicatelocyanobacteriumthalassaucyna AT jonathanpzehr transcriptionalcycleissuitedtodaytimensub2subfixationintheunicellularcyanobacteriumitalictoggleyescandidatusitalicatelocyanobacteriumthalassaucyna
_version_	1718427246708916224

The Transcriptional Cycle Is Suited to Daytime N<sub>2</sub> Fixation in the Unicellular Cyanobacterium “<italic toggle="yes">Candidatus</italic> Atelocyanobacterium thalassa” (UCYN-A)

Ejemplares similares