Direct Heme Uptake by Phytoplankton-Associated <italic toggle="yes">Roseobacter</italic> Bacteria

ABSTRACT Iron is an essential micronutrient and can limit the growth of both marine phytoplankton and heterotrophic bacterioplankton. In this study, we investigated the molecular basis of heme transport, an organic iron acquisition pathway, in phytoplankton-associated Roseobacter bacteria and explor...

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Autores principales:	Shane L. Hogle, Bianca Brahamsha, Katherine A. Barbeau
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2017
Materias:	roseobacter diatom algae phytoplankton-bacterium interactions marine iron transport Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/0d1f99470de6455e98efe695f65f0607
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spelling	oai:doaj.org-article:0d1f99470de6455e98efe695f65f06072021-12-02T19:45:29ZDirect Heme Uptake by Phytoplankton-Associated <italic toggle="yes">Roseobacter</italic> Bacteria10.1128/mSystems.00124-162379-5077https://doaj.org/article/0d1f99470de6455e98efe695f65f06072017-02-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00124-16https://doaj.org/toc/2379-5077ABSTRACT Iron is an essential micronutrient and can limit the growth of both marine phytoplankton and heterotrophic bacterioplankton. In this study, we investigated the molecular basis of heme transport, an organic iron acquisition pathway, in phytoplankton-associated Roseobacter bacteria and explored the potential role of bacterial heme uptake in the marine environment. We searched 153 Roseobacter genomes and found that nearly half contained putative complete heme transport systems with nearly the same synteny. We also examined a publicly available coculture transcriptome and found that Roseobacter strain Sulfitobacter sp. strain SA11 strongly downregulated a putative heme transport gene cluster during mutualistic growth with a marine diatom, suggesting that the regulation of heme transport might be influenced by host cues. We generated a mutant of phytoplankton-associated Roseobacter strain Ruegeria sp. strain TM1040 by insertionally inactivating its homolog of the TonB-dependent heme transporter hmuR and confirmed the role of this gene in the uptake of heme and hemoproteins. We performed competition experiments between iron-limited wild-type and mutant TM1040 strains and found that the wild type maintains a growth advantage when competing with the mutant for iron compounds derived solely from lysed diatom cells. Heme transport systems were largely absent from public marine metagenomes and metatranscriptomes, suggesting that marine bacteria with the potential for heme transport likely have small standing populations in the free-living bacterioplankton. Heme transport is likely a useful strategy for phytoplankton-associated bacteria because it provides direct access to components of the host intracellular iron pool after lysis. IMPORTANCE Ecosystem productivity in large regions of the surface ocean is fueled by iron that has been microbially regenerated from biomass. Currently, the specific microbes and molecules that mediate the transfer of recycled iron between microbial trophic levels remain largely unknown. We characterized a marine bacterial heme transporter and verified its role in acquiring heme, an abundant iron-containing enzyme cofactor. We present evidence that after host cell lysis, phytoplankton-associated bacteria directly extract heme and hemoproteins from algal cellular debris in order to fulfill their iron requirements and that the regulation of this process may be modulated by host cues. Direct heme transport, in contrast to multistep extracellular processing of hemoproteins, may allow certain phytoplankton-associated bacteria to rapidly extract iron from decaying phytoplankton, thus efficiently recycling cellular iron into the wider microbial loop.Shane L. HogleBianca BrahamshaKatherine A. BarbeauAmerican Society for Microbiologyarticleroseobacterdiatomalgaephytoplankton-bacterium interactionsmarineiron transportMicrobiologyQR1-502ENmSystems, Vol 2, Iss 1 (2017)
institution	DOAJ
collection	DOAJ
language	EN
topic	roseobacter diatom algae phytoplankton-bacterium interactions marine iron transport Microbiology QR1-502
spellingShingle	roseobacter diatom algae phytoplankton-bacterium interactions marine iron transport Microbiology QR1-502 Shane L. Hogle Bianca Brahamsha Katherine A. Barbeau Direct Heme Uptake by Phytoplankton-Associated <italic toggle="yes">Roseobacter</italic> Bacteria
description	ABSTRACT Iron is an essential micronutrient and can limit the growth of both marine phytoplankton and heterotrophic bacterioplankton. In this study, we investigated the molecular basis of heme transport, an organic iron acquisition pathway, in phytoplankton-associated Roseobacter bacteria and explored the potential role of bacterial heme uptake in the marine environment. We searched 153 Roseobacter genomes and found that nearly half contained putative complete heme transport systems with nearly the same synteny. We also examined a publicly available coculture transcriptome and found that Roseobacter strain Sulfitobacter sp. strain SA11 strongly downregulated a putative heme transport gene cluster during mutualistic growth with a marine diatom, suggesting that the regulation of heme transport might be influenced by host cues. We generated a mutant of phytoplankton-associated Roseobacter strain Ruegeria sp. strain TM1040 by insertionally inactivating its homolog of the TonB-dependent heme transporter hmuR and confirmed the role of this gene in the uptake of heme and hemoproteins. We performed competition experiments between iron-limited wild-type and mutant TM1040 strains and found that the wild type maintains a growth advantage when competing with the mutant for iron compounds derived solely from lysed diatom cells. Heme transport systems were largely absent from public marine metagenomes and metatranscriptomes, suggesting that marine bacteria with the potential for heme transport likely have small standing populations in the free-living bacterioplankton. Heme transport is likely a useful strategy for phytoplankton-associated bacteria because it provides direct access to components of the host intracellular iron pool after lysis. IMPORTANCE Ecosystem productivity in large regions of the surface ocean is fueled by iron that has been microbially regenerated from biomass. Currently, the specific microbes and molecules that mediate the transfer of recycled iron between microbial trophic levels remain largely unknown. We characterized a marine bacterial heme transporter and verified its role in acquiring heme, an abundant iron-containing enzyme cofactor. We present evidence that after host cell lysis, phytoplankton-associated bacteria directly extract heme and hemoproteins from algal cellular debris in order to fulfill their iron requirements and that the regulation of this process may be modulated by host cues. Direct heme transport, in contrast to multistep extracellular processing of hemoproteins, may allow certain phytoplankton-associated bacteria to rapidly extract iron from decaying phytoplankton, thus efficiently recycling cellular iron into the wider microbial loop.
format	article
author	Shane L. Hogle Bianca Brahamsha Katherine A. Barbeau
author_facet	Shane L. Hogle Bianca Brahamsha Katherine A. Barbeau
author_sort	Shane L. Hogle
title	Direct Heme Uptake by Phytoplankton-Associated <italic toggle="yes">Roseobacter</italic> Bacteria
title_short	Direct Heme Uptake by Phytoplankton-Associated <italic toggle="yes">Roseobacter</italic> Bacteria
title_full	Direct Heme Uptake by Phytoplankton-Associated <italic toggle="yes">Roseobacter</italic> Bacteria
title_fullStr	Direct Heme Uptake by Phytoplankton-Associated <italic toggle="yes">Roseobacter</italic> Bacteria
title_full_unstemmed	Direct Heme Uptake by Phytoplankton-Associated <italic toggle="yes">Roseobacter</italic> Bacteria
title_sort	direct heme uptake by phytoplankton-associated <italic toggle="yes">roseobacter</italic> bacteria
publisher	American Society for Microbiology
publishDate	2017
url	https://doaj.org/article/0d1f99470de6455e98efe695f65f0607
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Direct Heme Uptake by Phytoplankton-Associated <italic toggle="yes">Roseobacter</italic> Bacteria

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