Proteome Remodeling in Response to Sulfur Limitation in “<italic toggle="yes">Candidatus</italic> Pelagibacter ubique”

ABSTRACT The alphaproteobacterium “Candidatus Pelagibacter ubique” strain HTCC1062 and most other members of the SAR11 clade lack genes for assimilatory sulfate reduction, making them dependent on organosulfur compounds that occur naturally in seawater. To investigate how these cells adapt to sulfur...

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Autores principales:	Daniel P. Smith, Carrie D. Nicora, Paul Carini, Mary S. Lipton, Angela D. Norbeck, Richard D. Smith, Stephen J. Giovannoni
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2016
Materias:	SAR11 regulation riboswitch transcriptome Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/74331e1816284d6d878300b3d7815177
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spelling	oai:doaj.org-article:74331e1816284d6d878300b3d78151772021-12-02T18:39:33ZProteome Remodeling in Response to Sulfur Limitation in “<italic toggle="yes">Candidatus</italic> Pelagibacter ubique”10.1128/mSystems.00068-162379-5077https://doaj.org/article/74331e1816284d6d878300b3d78151772016-08-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00068-16https://doaj.org/toc/2379-5077ABSTRACT The alphaproteobacterium “Candidatus Pelagibacter ubique” strain HTCC1062 and most other members of the SAR11 clade lack genes for assimilatory sulfate reduction, making them dependent on organosulfur compounds that occur naturally in seawater. To investigate how these cells adapt to sulfur limitation, batch cultures were grown in defined medium containing either limiting or nonlimiting amounts of dimethylsulfoniopropionate (DMSP) as the sole sulfur source. Protein and mRNA expression were measured before, during, and after the transition from exponential growth to stationary phase. Two distinct responses were observed, one as DMSP became exhausted and another as the cells acclimated to a sulfur-limited environment. The first response was characterized by increased transcription and translation of all “Ca. Pelagibacter ubique” genes downstream from the previously confirmed S-adenosyl methionine (SAM) riboswitches bhmT, mmuM, and metY. The proteins encoded by these genes were up to 33 times more abundant as DMSP became limiting. Their predicted function is to shunt all available sulfur to methionine. The secondary response, observed during sulfur-limited stationary phase, was a 6- to 10-fold increase in the transcription of the heme c shuttle-encoding gene ccmC and two small genes of unknown function (SAR11_1163 and SAR11_1164). This bacterium’s strategy for coping with sulfur stress appears to be intracellular redistribution to support methionine biosynthesis rather than increasing organosulfur import. Many of the genes and SAM riboswitches involved in this response are located in a hypervariable genome region (HVR). One of these HVR genes, ordL, is located downstream from a conserved motif that evidence suggests is a novel riboswitch. IMPORTANCE “Ca. Pelagibacter ubique” is a key driver of marine biogeochemistry cycles and a model for understanding how minimal genomes evolved in free-living anucleate organisms. This study explores the unusual sulfur acquisition strategy that has evolved in these cells, which lack assimilatory sulfate reduction and instead rely on reduced sulfur compounds found in oxic marine environments to meet their cellular quotas. Our findings demonstrate that the sulfur acquisition systems are constitutively expressed but the enzymatic steps leading to the essential sulfur-containing amino acid methionine are regulated by a unique array of riboswitches and genes, many of which are encoded in a rapidly evolving genome region. These findings support mounting evidence that streamlined cells have evolved regulatory mechanisms that minimize transcriptional switching and, unexpectedly, localize essential sulfur acquisition genes in a genome region normally associated with adaption to environmental variation.Daniel P. SmithCarrie D. NicoraPaul CariniMary S. LiptonAngela D. NorbeckRichard D. SmithStephen J. GiovannoniAmerican Society for MicrobiologyarticleSAR11regulationriboswitchtranscriptomeMicrobiologyQR1-502ENmSystems, Vol 1, Iss 4 (2016)
institution	DOAJ
collection	DOAJ
language	EN
topic	SAR11 regulation riboswitch transcriptome Microbiology QR1-502
spellingShingle	SAR11 regulation riboswitch transcriptome Microbiology QR1-502 Daniel P. Smith Carrie D. Nicora Paul Carini Mary S. Lipton Angela D. Norbeck Richard D. Smith Stephen J. Giovannoni Proteome Remodeling in Response to Sulfur Limitation in “<italic toggle="yes">Candidatus</italic> Pelagibacter ubique”
description	ABSTRACT The alphaproteobacterium “Candidatus Pelagibacter ubique” strain HTCC1062 and most other members of the SAR11 clade lack genes for assimilatory sulfate reduction, making them dependent on organosulfur compounds that occur naturally in seawater. To investigate how these cells adapt to sulfur limitation, batch cultures were grown in defined medium containing either limiting or nonlimiting amounts of dimethylsulfoniopropionate (DMSP) as the sole sulfur source. Protein and mRNA expression were measured before, during, and after the transition from exponential growth to stationary phase. Two distinct responses were observed, one as DMSP became exhausted and another as the cells acclimated to a sulfur-limited environment. The first response was characterized by increased transcription and translation of all “Ca. Pelagibacter ubique” genes downstream from the previously confirmed S-adenosyl methionine (SAM) riboswitches bhmT, mmuM, and metY. The proteins encoded by these genes were up to 33 times more abundant as DMSP became limiting. Their predicted function is to shunt all available sulfur to methionine. The secondary response, observed during sulfur-limited stationary phase, was a 6- to 10-fold increase in the transcription of the heme c shuttle-encoding gene ccmC and two small genes of unknown function (SAR11_1163 and SAR11_1164). This bacterium’s strategy for coping with sulfur stress appears to be intracellular redistribution to support methionine biosynthesis rather than increasing organosulfur import. Many of the genes and SAM riboswitches involved in this response are located in a hypervariable genome region (HVR). One of these HVR genes, ordL, is located downstream from a conserved motif that evidence suggests is a novel riboswitch. IMPORTANCE “Ca. Pelagibacter ubique” is a key driver of marine biogeochemistry cycles and a model for understanding how minimal genomes evolved in free-living anucleate organisms. This study explores the unusual sulfur acquisition strategy that has evolved in these cells, which lack assimilatory sulfate reduction and instead rely on reduced sulfur compounds found in oxic marine environments to meet their cellular quotas. Our findings demonstrate that the sulfur acquisition systems are constitutively expressed but the enzymatic steps leading to the essential sulfur-containing amino acid methionine are regulated by a unique array of riboswitches and genes, many of which are encoded in a rapidly evolving genome region. These findings support mounting evidence that streamlined cells have evolved regulatory mechanisms that minimize transcriptional switching and, unexpectedly, localize essential sulfur acquisition genes in a genome region normally associated with adaption to environmental variation.
format	article
author	Daniel P. Smith Carrie D. Nicora Paul Carini Mary S. Lipton Angela D. Norbeck Richard D. Smith Stephen J. Giovannoni
author_facet	Daniel P. Smith Carrie D. Nicora Paul Carini Mary S. Lipton Angela D. Norbeck Richard D. Smith Stephen J. Giovannoni
author_sort	Daniel P. Smith
title	Proteome Remodeling in Response to Sulfur Limitation in “<italic toggle="yes">Candidatus</italic> Pelagibacter ubique”
title_short	Proteome Remodeling in Response to Sulfur Limitation in “<italic toggle="yes">Candidatus</italic> Pelagibacter ubique”
title_full	Proteome Remodeling in Response to Sulfur Limitation in “<italic toggle="yes">Candidatus</italic> Pelagibacter ubique”
title_fullStr	Proteome Remodeling in Response to Sulfur Limitation in “<italic toggle="yes">Candidatus</italic> Pelagibacter ubique”
title_full_unstemmed	Proteome Remodeling in Response to Sulfur Limitation in “<italic toggle="yes">Candidatus</italic> Pelagibacter ubique”
title_sort	proteome remodeling in response to sulfur limitation in “<italic toggle="yes">candidatus</italic> pelagibacter ubique”
publisher	American Society for Microbiology
publishDate	2016
url	https://doaj.org/article/74331e1816284d6d878300b3d7815177
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Proteome Remodeling in Response to Sulfur Limitation in “<italic toggle="yes">Candidatus</italic> Pelagibacter ubique”

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