Marine Fungi Select and Transport Aerobic and Anaerobic Bacterial Populations from Polycyclic Aromatic Hydrocarbon-Contaminated Sediments

ABSTRACT The organization of microbial communities in marine sediment relies on complex biotic and abiotic interactions. Among them, the interaction between fungi and bacteria plays a crucial role building specific microbial assemblages, resulting in metabolic networks adapted to environmental condi...

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Main Authors: Joyce Álvarez-Barragán, Cristiana Cravo-Laureau, Bijing Xiong, Lukas Y. Wick, Robert Duran
Format: Article
Language:English
Published: American Society for Microbiology 2023-04-01
Series:mBio
Subjects:
Online Access:https://journals.asm.org/doi/10.1128/mbio.02761-22
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author Joyce Álvarez-Barragán
Cristiana Cravo-Laureau
Bijing Xiong
Lukas Y. Wick
Robert Duran
author_facet Joyce Álvarez-Barragán
Cristiana Cravo-Laureau
Bijing Xiong
Lukas Y. Wick
Robert Duran
author_sort Joyce Álvarez-Barragán
collection DOAJ
description ABSTRACT The organization of microbial communities in marine sediment relies on complex biotic and abiotic interactions. Among them, the interaction between fungi and bacteria plays a crucial role building specific microbial assemblages, resulting in metabolic networks adapted to environmental conditions. The fungal-bacterial interaction (FBI) includes bacterial translocation via fungal mycelia, allowing bacterial dispersion, and ecological niche colonization. In order to demonstrate that the translocation of bacteria through fungal mycelia involves bacterial selection, the mycelia of two fungi isolated from marine coastal sediment, Alternaria destruens F10.81 and Fusarium pseudonygamai F5.76, showing different strategies for uptake of polycyclic aromatic hydrocarbon (PAH), homogenous internalization and vacuole forming respectively, were used to translocate bacteria through hydrophobic hydrocarbon contaminated sediments. A. destruens F10.81 selected four specific bacteria, while bacterial selection by F. pseudonygamai F5.76 was not evident. Among the bacteria selected by A. destruens F10.81, Spirochaeta litoralis, known as strictly anaerobic bacterium, was identified, indicating that A. destruens F10.81 selects and transports both aerobic and anaerobic bacteria. Such a result is consistent with the observed formation of anoxic micro-niches in areas surrounding and affected by fungal hyphae. Our findings provide new insights on the selection and dispersion of bacterial communities by fungi, which are crucial for the organization of microbial communities and their functioning in coastal PAH-contaminated sediments. IMPORTANCE The study provides advances for understanding fungal-bacterial relationships, particularly on the selection and dispersion of bacterial communities by fungi, which are crucial for the organization of microbial communities and their functioning in coastal PAH-contaminated sediments. The transportation of bacteria via fungal hyphae (fungal highway) results in bacterial selection; in particular, fungal hyphae offer adequate conditions for the transport of both aerobic and anaerobic bacteria through hydrophobic patches for the colonization of novel niches.
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spelling doaj.art-04ee954381894b5dbf6047e65f706eb02024-08-11T18:27:31ZengAmerican Society for MicrobiologymBio2150-75112023-04-0114210.1128/mbio.02761-22Marine Fungi Select and Transport Aerobic and Anaerobic Bacterial Populations from Polycyclic Aromatic Hydrocarbon-Contaminated SedimentsJoyce Álvarez-Barragán0Cristiana Cravo-Laureau1Bijing Xiong2Lukas Y. Wick3Robert Duran4Universite de Pau et des Pays de l’Adour, E2S UPPA, CNRS, IPREM, Pau, FranceUniversite de Pau et des Pays de l’Adour, E2S UPPA, CNRS, IPREM, Pau, FranceHelmholtz Centre for Environmental Research–UFZ, Department of Environmental Microbiology, Leipzig, GermanyHelmholtz Centre for Environmental Research–UFZ, Department of Environmental Microbiology, Leipzig, GermanyUniversite de Pau et des Pays de l’Adour, E2S UPPA, CNRS, IPREM, Pau, FranceABSTRACT The organization of microbial communities in marine sediment relies on complex biotic and abiotic interactions. Among them, the interaction between fungi and bacteria plays a crucial role building specific microbial assemblages, resulting in metabolic networks adapted to environmental conditions. The fungal-bacterial interaction (FBI) includes bacterial translocation via fungal mycelia, allowing bacterial dispersion, and ecological niche colonization. In order to demonstrate that the translocation of bacteria through fungal mycelia involves bacterial selection, the mycelia of two fungi isolated from marine coastal sediment, Alternaria destruens F10.81 and Fusarium pseudonygamai F5.76, showing different strategies for uptake of polycyclic aromatic hydrocarbon (PAH), homogenous internalization and vacuole forming respectively, were used to translocate bacteria through hydrophobic hydrocarbon contaminated sediments. A. destruens F10.81 selected four specific bacteria, while bacterial selection by F. pseudonygamai F5.76 was not evident. Among the bacteria selected by A. destruens F10.81, Spirochaeta litoralis, known as strictly anaerobic bacterium, was identified, indicating that A. destruens F10.81 selects and transports both aerobic and anaerobic bacteria. Such a result is consistent with the observed formation of anoxic micro-niches in areas surrounding and affected by fungal hyphae. Our findings provide new insights on the selection and dispersion of bacterial communities by fungi, which are crucial for the organization of microbial communities and their functioning in coastal PAH-contaminated sediments. IMPORTANCE The study provides advances for understanding fungal-bacterial relationships, particularly on the selection and dispersion of bacterial communities by fungi, which are crucial for the organization of microbial communities and their functioning in coastal PAH-contaminated sediments. The transportation of bacteria via fungal hyphae (fungal highway) results in bacterial selection; in particular, fungal hyphae offer adequate conditions for the transport of both aerobic and anaerobic bacteria through hydrophobic patches for the colonization of novel niches.https://journals.asm.org/doi/10.1128/mbio.02761-22fungal translocation networkfungal-bacterial interactionshyphal selectionoxygen consumptionbacterial diversitybacteria dispersion
spellingShingle Joyce Álvarez-Barragán
Cristiana Cravo-Laureau
Bijing Xiong
Lukas Y. Wick
Robert Duran
Marine Fungi Select and Transport Aerobic and Anaerobic Bacterial Populations from Polycyclic Aromatic Hydrocarbon-Contaminated Sediments
mBio
fungal translocation network
fungal-bacterial interactions
hyphal selection
oxygen consumption
bacterial diversity
bacteria dispersion
title Marine Fungi Select and Transport Aerobic and Anaerobic Bacterial Populations from Polycyclic Aromatic Hydrocarbon-Contaminated Sediments
title_full Marine Fungi Select and Transport Aerobic and Anaerobic Bacterial Populations from Polycyclic Aromatic Hydrocarbon-Contaminated Sediments
title_fullStr Marine Fungi Select and Transport Aerobic and Anaerobic Bacterial Populations from Polycyclic Aromatic Hydrocarbon-Contaminated Sediments
title_full_unstemmed Marine Fungi Select and Transport Aerobic and Anaerobic Bacterial Populations from Polycyclic Aromatic Hydrocarbon-Contaminated Sediments
title_short Marine Fungi Select and Transport Aerobic and Anaerobic Bacterial Populations from Polycyclic Aromatic Hydrocarbon-Contaminated Sediments
title_sort marine fungi select and transport aerobic and anaerobic bacterial populations from polycyclic aromatic hydrocarbon contaminated sediments
topic fungal translocation network
fungal-bacterial interactions
hyphal selection
oxygen consumption
bacterial diversity
bacteria dispersion
url https://journals.asm.org/doi/10.1128/mbio.02761-22
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