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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| Format: | Article |
| Language: | English |
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American Society for Microbiology
2017-02-01
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| Series: | mSystems |
| Subjects: | |
| Online Access: | https://journals.asm.org/doi/10.1128/mSystems.00124-16 |
| _version_ | 1818405888346554368 |
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| author | Shane L. Hogle Bianca Brahamsha Katherine A. Barbeau |
| author_facet | Shane L. Hogle Bianca Brahamsha Katherine A. Barbeau |
| author_sort | Shane L. Hogle |
| collection | DOAJ |
| 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. |
| first_indexed | 2024-12-14T09:03:12Z |
| format | Article |
| id | doaj.art-0d1f99470de6455e98efe695f65f0607 |
| institution | Directory Open Access Journal |
| issn | 2379-5077 |
| language | English |
| last_indexed | 2024-12-14T09:03:12Z |
| publishDate | 2017-02-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | mSystems |
| spelling | doaj.art-0d1f99470de6455e98efe695f65f06072022-12-21T23:08:46ZengAmerican Society for MicrobiologymSystems2379-50772017-02-012110.1128/mSystems.00124-16Direct Heme Uptake by Phytoplankton-Associated <italic toggle="yes">Roseobacter</italic> BacteriaShane L. Hogle0Bianca Brahamsha1Katherine A. Barbeau2Geosciences Research Division, Scripps Institution of Oceanography, La Jolla, California, USAMarine Biology Research Division, Scripps Institution of Oceanography, La Jolla, California, USAGeosciences Research Division, Scripps Institution of Oceanography, La Jolla, California, USAABSTRACT 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.https://journals.asm.org/doi/10.1128/mSystems.00124-16roseobacterdiatomalgaephytoplankton-bacterium interactionsmarineiron transport |
| spellingShingle | Shane L. Hogle Bianca Brahamsha Katherine A. Barbeau Direct Heme Uptake by Phytoplankton-Associated <italic toggle="yes">Roseobacter</italic> Bacteria mSystems roseobacter diatom algae phytoplankton-bacterium interactions marine iron transport |
| title | 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_short | 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 |
| topic | roseobacter diatom algae phytoplankton-bacterium interactions marine iron transport |
| url | https://journals.asm.org/doi/10.1128/mSystems.00124-16 |
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