Transcriptomic Study of Substrate-Specific Transport Mechanisms for Iron and Carbon in the Marine Copiotroph <named-content content-type="genus-species">Alteromonas macleodii</named-content>

ABSTRACT Iron is an essential micronutrient for all microbial growth in the marine environment, and in heterotrophic bacteria, iron is tightly linked to carbon metabolism due to its central role as a cofactor in enzymes of the respiratory chain. Here, we present the iron- and carbon-regulated transc...

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Autores principales:	Lauren E. Manck, Josh L. Espinoza, Christopher L. Dupont, Katherine A. Barbeau
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2020
Materias:	Alteromonas TonB carbon transport gene expression iron transport marine microbiology Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/c69c209ee765487ab5061c4dd50d318a
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spelling	oai:doaj.org-article:c69c209ee765487ab5061c4dd50d318a2021-12-02T19:46:20ZTranscriptomic Study of Substrate-Specific Transport Mechanisms for Iron and Carbon in the Marine Copiotroph <named-content content-type="genus-species">Alteromonas macleodii</named-content>10.1128/mSystems.00070-202379-5077https://doaj.org/article/c69c209ee765487ab5061c4dd50d318a2020-04-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00070-20https://doaj.org/toc/2379-5077ABSTRACT Iron is an essential micronutrient for all microbial growth in the marine environment, and in heterotrophic bacteria, iron is tightly linked to carbon metabolism due to its central role as a cofactor in enzymes of the respiratory chain. Here, we present the iron- and carbon-regulated transcriptomes of a representative marine copiotroph, Alteromonas macleodii ATCC 27126, and characterize its cellular transport mechanisms. ATCC 27126 has distinct metabolic responses to iron and carbon limitation and, accordingly, uses distinct sets of TonB-dependent transporters for the acquisition of iron and carbon. These distinct sets of TonB-dependent transporters were of a similar number, indicating that the diversity of carbon and iron substrates available to ATCC 27126 is of a similar scale. For the first time in a marine bacterium, we have also identified six characteristic inner membrane permeases for the transport of siderophores via an ATPase-independent mechanism. An examination of the distribution of specific TonB-dependent transporters in 31 genomes across the genus Alteromonas points to niche specialization in transport capacity, particularly for iron. We conclude that the substrate-specific bioavailability of both iron and carbon in the marine environment will likely be a key control on the processing of organic matter through the microbial loop. IMPORTANCE As the major facilitators of the turnover of organic matter in the marine environment, the ability of heterotrophic bacteria to acquire specific compounds within the diverse range of dissolved organic matter will affect the regeneration of essential nutrients such as iron and carbon. TonB-dependent transporters are a prevalent cellular tool in Gram-negative bacteria that allow a relatively high-molecular-weight fraction of organic matter to be directly accessed. However, these transporters are not well characterized in marine bacteria, limiting our understanding of the flow of specific substrates through the marine microbial loop. Here, we characterize the TonB-dependent transporters responsible for iron and carbon acquisition in a representative marine copiotroph and examine their distribution across the genus Alteromonas. We provide evidence that substrate-specific bioavailability is niche specific, particularly for iron complexes, indicating that transport capacity may serve as a significant control on microbial community dynamics and the resultant cycling of organic matter.Lauren E. ManckJosh L. EspinozaChristopher L. DupontKatherine A. BarbeauAmerican Society for MicrobiologyarticleAlteromonasTonBcarbon transportgene expressioniron transportmarine microbiologyMicrobiologyQR1-502ENmSystems, Vol 5, Iss 2 (2020)
institution	DOAJ
collection	DOAJ
language	EN
topic	Alteromonas TonB carbon transport gene expression iron transport marine microbiology Microbiology QR1-502
spellingShingle	Alteromonas TonB carbon transport gene expression iron transport marine microbiology Microbiology QR1-502 Lauren E. Manck Josh L. Espinoza Christopher L. Dupont Katherine A. Barbeau Transcriptomic Study of Substrate-Specific Transport Mechanisms for Iron and Carbon in the Marine Copiotroph <named-content content-type="genus-species">Alteromonas macleodii</named-content>
description	ABSTRACT Iron is an essential micronutrient for all microbial growth in the marine environment, and in heterotrophic bacteria, iron is tightly linked to carbon metabolism due to its central role as a cofactor in enzymes of the respiratory chain. Here, we present the iron- and carbon-regulated transcriptomes of a representative marine copiotroph, Alteromonas macleodii ATCC 27126, and characterize its cellular transport mechanisms. ATCC 27126 has distinct metabolic responses to iron and carbon limitation and, accordingly, uses distinct sets of TonB-dependent transporters for the acquisition of iron and carbon. These distinct sets of TonB-dependent transporters were of a similar number, indicating that the diversity of carbon and iron substrates available to ATCC 27126 is of a similar scale. For the first time in a marine bacterium, we have also identified six characteristic inner membrane permeases for the transport of siderophores via an ATPase-independent mechanism. An examination of the distribution of specific TonB-dependent transporters in 31 genomes across the genus Alteromonas points to niche specialization in transport capacity, particularly for iron. We conclude that the substrate-specific bioavailability of both iron and carbon in the marine environment will likely be a key control on the processing of organic matter through the microbial loop. IMPORTANCE As the major facilitators of the turnover of organic matter in the marine environment, the ability of heterotrophic bacteria to acquire specific compounds within the diverse range of dissolved organic matter will affect the regeneration of essential nutrients such as iron and carbon. TonB-dependent transporters are a prevalent cellular tool in Gram-negative bacteria that allow a relatively high-molecular-weight fraction of organic matter to be directly accessed. However, these transporters are not well characterized in marine bacteria, limiting our understanding of the flow of specific substrates through the marine microbial loop. Here, we characterize the TonB-dependent transporters responsible for iron and carbon acquisition in a representative marine copiotroph and examine their distribution across the genus Alteromonas. We provide evidence that substrate-specific bioavailability is niche specific, particularly for iron complexes, indicating that transport capacity may serve as a significant control on microbial community dynamics and the resultant cycling of organic matter.
format	article
author	Lauren E. Manck Josh L. Espinoza Christopher L. Dupont Katherine A. Barbeau
author_facet	Lauren E. Manck Josh L. Espinoza Christopher L. Dupont Katherine A. Barbeau
author_sort	Lauren E. Manck
title	Transcriptomic Study of Substrate-Specific Transport Mechanisms for Iron and Carbon in the Marine Copiotroph <named-content content-type="genus-species">Alteromonas macleodii</named-content>
title_short	Transcriptomic Study of Substrate-Specific Transport Mechanisms for Iron and Carbon in the Marine Copiotroph <named-content content-type="genus-species">Alteromonas macleodii</named-content>
title_full	Transcriptomic Study of Substrate-Specific Transport Mechanisms for Iron and Carbon in the Marine Copiotroph <named-content content-type="genus-species">Alteromonas macleodii</named-content>
title_fullStr	Transcriptomic Study of Substrate-Specific Transport Mechanisms for Iron and Carbon in the Marine Copiotroph <named-content content-type="genus-species">Alteromonas macleodii</named-content>
title_full_unstemmed	Transcriptomic Study of Substrate-Specific Transport Mechanisms for Iron and Carbon in the Marine Copiotroph <named-content content-type="genus-species">Alteromonas macleodii</named-content>
title_sort	transcriptomic study of substrate-specific transport mechanisms for iron and carbon in the marine copiotroph <named-content content-type="genus-species">alteromonas macleodii</named-content>
publisher	American Society for Microbiology
publishDate	2020
url	https://doaj.org/article/c69c209ee765487ab5061c4dd50d318a
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Transcriptomic Study of Substrate-Specific Transport Mechanisms for Iron and Carbon in the Marine Copiotroph <named-content content-type="genus-species">Alteromonas macleodii</named-content>

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