Geobacter-associated prophages confer beneficial effect on dissimilatory reduction of Fe(III) oxides

The dissimilatory reduction of Fe(III) oxides driven by Fe(III)-reducing bacteria (FRB) is an important biogeochemical process that influences not only iron cycling but also the biogeochemical cycles of carbon, trace metals, nutrients and contaminants. Phages have central roles in modulating the pop...

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Main Authors: Guiqin Yang, Annian Lin, Xian Wu, Canfen Lin, Siyue Zhu, Li Zhuang
Format: Article
Language:English
Published: KeAi Communications Co. Ltd. 2024-11-01
Series:Fundamental Research
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Online Access:http://www.sciencedirect.com/science/article/pii/S2667325822004277
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author Guiqin Yang
Annian Lin
Xian Wu
Canfen Lin
Siyue Zhu
Li Zhuang
author_facet Guiqin Yang
Annian Lin
Xian Wu
Canfen Lin
Siyue Zhu
Li Zhuang
author_sort Guiqin Yang
collection DOAJ
description The dissimilatory reduction of Fe(III) oxides driven by Fe(III)-reducing bacteria (FRB) is an important biogeochemical process that influences not only iron cycling but also the biogeochemical cycles of carbon, trace metals, nutrients and contaminants. Phages have central roles in modulating the population and activity of FRB, but the mechanism for phage-involved Fe(III) oxide reduction is still unclear. This work used a common FRB, Geobacter soli, to explore the roles and underlying mechanisms of FRB-harboring prophages in the dissimilatory reduction of Fe(III) oxides. Bioinformatic analysis predicted 185 phage-related genes in the G. soli genome, comprising functional prophages that were verified to be induced to form tailed phage particles. Ferrihydrite reduction was facilitated as prophage induction was stimulated and declined as prophage induction was inhibited, which indicated a positive role of G. soli-harboring prophages in Fe(III) oxide reduction. A comparison of gene expression and released phage particles in the cells grown with Fe(III)-citrate and ferrihydrite suggested that microbial ferrihydrite reduction would activate the SOS response and consequently induce the prophages to enter lytic cycles. The prophage-mediated lysis of the subpopulation resulted in an increased release of extracellular DNA and membrane vesicles that were conducive to Fe(III) oxide reduction, which might explain the positive role of prophages in ferrihydrite reduction. In summary, our results revealed the functional roles and underlying mechanisms of FRB-associated prophages in facilitating the dissimilatory reduction of Fe(III) oxides, which will advance our understanding of iron cycling in natural ecosystems.
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spelling doaj-art-a0ceb439dd8847a3a498fbe9b0eddc672024-12-01T05:08:47ZengKeAi Communications Co. Ltd.Fundamental Research2667-32582024-11-014615681575Geobacter-associated prophages confer beneficial effect on dissimilatory reduction of Fe(III) oxidesGuiqin Yang0Annian Lin1Xian Wu2Canfen Lin3Siyue Zhu4Li Zhuang5Guangdong Key Laboratory of Environmental Pollution and Health, School of Environment, Jinan University, Guangzhou 510632, ChinaGuangdong Key Laboratory of Environmental Pollution and Health, School of Environment, Jinan University, Guangzhou 510632, ChinaGuangdong Key Laboratory of Environmental Pollution and Health, School of Environment, Jinan University, Guangzhou 510632, ChinaGuangdong Key Laboratory of Environmental Pollution and Health, School of Environment, Jinan University, Guangzhou 510632, ChinaGuangdong Key Laboratory of Environmental Pollution and Health, School of Environment, Jinan University, Guangzhou 510632, ChinaCorresponding author.; Guangdong Key Laboratory of Environmental Pollution and Health, School of Environment, Jinan University, Guangzhou 510632, ChinaThe dissimilatory reduction of Fe(III) oxides driven by Fe(III)-reducing bacteria (FRB) is an important biogeochemical process that influences not only iron cycling but also the biogeochemical cycles of carbon, trace metals, nutrients and contaminants. Phages have central roles in modulating the population and activity of FRB, but the mechanism for phage-involved Fe(III) oxide reduction is still unclear. This work used a common FRB, Geobacter soli, to explore the roles and underlying mechanisms of FRB-harboring prophages in the dissimilatory reduction of Fe(III) oxides. Bioinformatic analysis predicted 185 phage-related genes in the G. soli genome, comprising functional prophages that were verified to be induced to form tailed phage particles. Ferrihydrite reduction was facilitated as prophage induction was stimulated and declined as prophage induction was inhibited, which indicated a positive role of G. soli-harboring prophages in Fe(III) oxide reduction. A comparison of gene expression and released phage particles in the cells grown with Fe(III)-citrate and ferrihydrite suggested that microbial ferrihydrite reduction would activate the SOS response and consequently induce the prophages to enter lytic cycles. The prophage-mediated lysis of the subpopulation resulted in an increased release of extracellular DNA and membrane vesicles that were conducive to Fe(III) oxide reduction, which might explain the positive role of prophages in ferrihydrite reduction. In summary, our results revealed the functional roles and underlying mechanisms of FRB-associated prophages in facilitating the dissimilatory reduction of Fe(III) oxides, which will advance our understanding of iron cycling in natural ecosystems.http://www.sciencedirect.com/science/article/pii/S2667325822004277Dissimilatory reduction of Fe(III) oxidesGeobacterProphage inductionSOS responseIron cycling
spellingShingle Guiqin Yang
Annian Lin
Xian Wu
Canfen Lin
Siyue Zhu
Li Zhuang
Geobacter-associated prophages confer beneficial effect on dissimilatory reduction of Fe(III) oxides
Fundamental Research
Dissimilatory reduction of Fe(III) oxides
Geobacter
Prophage induction
SOS response
Iron cycling
title Geobacter-associated prophages confer beneficial effect on dissimilatory reduction of Fe(III) oxides
title_full Geobacter-associated prophages confer beneficial effect on dissimilatory reduction of Fe(III) oxides
title_fullStr Geobacter-associated prophages confer beneficial effect on dissimilatory reduction of Fe(III) oxides
title_full_unstemmed Geobacter-associated prophages confer beneficial effect on dissimilatory reduction of Fe(III) oxides
title_short Geobacter-associated prophages confer beneficial effect on dissimilatory reduction of Fe(III) oxides
title_sort geobacter associated prophages confer beneficial effect on dissimilatory reduction of fe iii oxides
topic Dissimilatory reduction of Fe(III) oxides
Geobacter
Prophage induction
SOS response
Iron cycling
url http://www.sciencedirect.com/science/article/pii/S2667325822004277
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AT xianwu geobacterassociatedprophagesconferbeneficialeffectondissimilatoryreductionoffeiiioxides
AT canfenlin geobacterassociatedprophagesconferbeneficialeffectondissimilatoryreductionoffeiiioxides
AT siyuezhu geobacterassociatedprophagesconferbeneficialeffectondissimilatoryreductionoffeiiioxides
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