Photoferrotrophs Produce a PioAB Electron Conduit for Extracellular Electron Uptake

ABSTRACT Photoferrotrophy is a form of anoxygenic photosynthesis whereby bacteria utilize soluble or insoluble forms of ferrous iron as an electron donor to fix carbon dioxide using light energy. They can also use poised electrodes as their electron donor via phototrophic extracellular electron upta...

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Autores principales:	Dinesh Gupta, Molly C. Sutherland, Karthikeyan Rengasamy, J. Mark Meacham, Robert G. Kranz, Arpita Bose
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2019
Materias:	photoferrotrophy phototrophic EEU Rhodopseudomonas palustris TIE-1 decaheme cytochrome c Fe(II)-oxidation Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/0fc9d910441646119715d3f781b3a168
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spelling	oai:doaj.org-article:0fc9d910441646119715d3f781b3a1682021-11-15T15:54:47ZPhotoferrotrophs Produce a PioAB Electron Conduit for Extracellular Electron Uptake10.1128/mBio.02668-192150-7511https://doaj.org/article/0fc9d910441646119715d3f781b3a1682019-12-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.02668-19https://doaj.org/toc/2150-7511ABSTRACT Photoferrotrophy is a form of anoxygenic photosynthesis whereby bacteria utilize soluble or insoluble forms of ferrous iron as an electron donor to fix carbon dioxide using light energy. They can also use poised electrodes as their electron donor via phototrophic extracellular electron uptake (phototrophic EEU). The electron uptake mechanisms underlying these processes are not well understood. Using Rhodopseudomonas palustris TIE-1 as a model, we show that a single periplasmic decaheme cytochrome c, PioA, and an outer membrane porin, PioB, form a complex allowing extracellular electron uptake across the outer membrane from both soluble iron and poised electrodes. We observe that PioA undergoes postsecretory proteolysis of its N terminus to produce a shorter heme-attached PioA (holo-PioAC, where PioAC represents the C terminus of PioA), which can exist both freely in the periplasm and in a complex with PioB. The extended N-terminal peptide controls heme attachment, and its processing is required to produce wild-type levels of holo-PioAC and holo-PioACB complex. It is also conserved in PioA homologs from other phototrophs. The presence of PioAB in these organisms correlate with their ability to perform photoferrotrophy and phototrophic EEU. IMPORTANCE Some anoxygenic phototrophs use soluble iron, insoluble iron minerals (such as rust), or their proxies (poised electrodes) as electron donors for photosynthesis. However, the underlying electron uptake mechanisms are not well established. Here, we show that these phototrophs use a protein complex made of an outer membrane porin and a periplasmic decaheme cytochrome (electron transfer protein) to harvest electrons from both soluble iron and poised electrodes. This complex has two unique characteristics: (i) it lacks an extracellular cytochrome c, and (ii) the periplasmic decaheme cytochrome c undergoes proteolytic cleavage to produce a functional electron transfer protein. These characteristics are conserved in phototrophs harboring homologous proteins.Dinesh GuptaMolly C. SutherlandKarthikeyan RengasamyJ. Mark MeachamRobert G. KranzArpita BoseAmerican Society for Microbiologyarticlephotoferrotrophyphototrophic EEURhodopseudomonas palustris TIE-1decaheme cytochrome cFe(II)-oxidationMicrobiologyQR1-502ENmBio, Vol 10, Iss 6 (2019)
institution	DOAJ
collection	DOAJ
language	EN
topic	photoferrotrophy phototrophic EEU Rhodopseudomonas palustris TIE-1 decaheme cytochrome c Fe(II)-oxidation Microbiology QR1-502
spellingShingle	photoferrotrophy phototrophic EEU Rhodopseudomonas palustris TIE-1 decaheme cytochrome c Fe(II)-oxidation Microbiology QR1-502 Dinesh Gupta Molly C. Sutherland Karthikeyan Rengasamy J. Mark Meacham Robert G. Kranz Arpita Bose Photoferrotrophs Produce a PioAB Electron Conduit for Extracellular Electron Uptake
description	ABSTRACT Photoferrotrophy is a form of anoxygenic photosynthesis whereby bacteria utilize soluble or insoluble forms of ferrous iron as an electron donor to fix carbon dioxide using light energy. They can also use poised electrodes as their electron donor via phototrophic extracellular electron uptake (phototrophic EEU). The electron uptake mechanisms underlying these processes are not well understood. Using Rhodopseudomonas palustris TIE-1 as a model, we show that a single periplasmic decaheme cytochrome c, PioA, and an outer membrane porin, PioB, form a complex allowing extracellular electron uptake across the outer membrane from both soluble iron and poised electrodes. We observe that PioA undergoes postsecretory proteolysis of its N terminus to produce a shorter heme-attached PioA (holo-PioAC, where PioAC represents the C terminus of PioA), which can exist both freely in the periplasm and in a complex with PioB. The extended N-terminal peptide controls heme attachment, and its processing is required to produce wild-type levels of holo-PioAC and holo-PioACB complex. It is also conserved in PioA homologs from other phototrophs. The presence of PioAB in these organisms correlate with their ability to perform photoferrotrophy and phototrophic EEU. IMPORTANCE Some anoxygenic phototrophs use soluble iron, insoluble iron minerals (such as rust), or their proxies (poised electrodes) as electron donors for photosynthesis. However, the underlying electron uptake mechanisms are not well established. Here, we show that these phototrophs use a protein complex made of an outer membrane porin and a periplasmic decaheme cytochrome (electron transfer protein) to harvest electrons from both soluble iron and poised electrodes. This complex has two unique characteristics: (i) it lacks an extracellular cytochrome c, and (ii) the periplasmic decaheme cytochrome c undergoes proteolytic cleavage to produce a functional electron transfer protein. These characteristics are conserved in phototrophs harboring homologous proteins.
format	article
author	Dinesh Gupta Molly C. Sutherland Karthikeyan Rengasamy J. Mark Meacham Robert G. Kranz Arpita Bose
author_facet	Dinesh Gupta Molly C. Sutherland Karthikeyan Rengasamy J. Mark Meacham Robert G. Kranz Arpita Bose
author_sort	Dinesh Gupta
title	Photoferrotrophs Produce a PioAB Electron Conduit for Extracellular Electron Uptake
title_short	Photoferrotrophs Produce a PioAB Electron Conduit for Extracellular Electron Uptake
title_full	Photoferrotrophs Produce a PioAB Electron Conduit for Extracellular Electron Uptake
title_fullStr	Photoferrotrophs Produce a PioAB Electron Conduit for Extracellular Electron Uptake
title_full_unstemmed	Photoferrotrophs Produce a PioAB Electron Conduit for Extracellular Electron Uptake
title_sort	photoferrotrophs produce a pioab electron conduit for extracellular electron uptake
publisher	American Society for Microbiology
publishDate	2019
url	https://doaj.org/article/0fc9d910441646119715d3f781b3a168
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Photoferrotrophs Produce a PioAB Electron Conduit for Extracellular Electron Uptake

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