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Title: Effect of Endosymbiotic Bacteria on Fungal Resistance Toward Heavy Metals

Abstract

Most studies on metal removal or tolerance by fungi or bacteria focus on single isolates, without taking into consideration that some fungi in nature may be colonized by endobacteria. To address this knowledge gap, we investigated the tolerance and removal of diverse metals with two fungal species: Linnemannia elongata containing Burkholderia-related endobacteria and Benniella erionia containing Mollicute-related endobacteria. Isogenic lines of both species were generated with antibiotic treatments to remove their respective endobacteria. Experiments involved comparing the isogenic lines and wild type fungi in relation to the minimum inhibitory concentration for the metals, the fungal ability to remove these different metals via atomic adsorption spectroscopy, and the interaction of the metals with specific functional groups of the fungi and fungi-bacteria to determine the role of the bacteria via attenuated total reflection fourier transformed infrared (ATR-FTIR). Finally, we determined the influence of different metal concentrations, associated with moderate and high fungal growth inhibition, on the presence of the endobacteria inside the fungal mycelium via quantitative real-time PCR. Results showed that the presence of the endosymbiont increased B. erionia resistance to Mn 2+ and increased the removal of Fe 2+ compared to isogenic lines. The absence of the endosymbiont in L. elongatamore » increased the fungal resistance toward Fe 2+ and improved the removal of Fe 2+ . Furthermore, when the bacterial endosymbiont was present in L. elongata , a decrease in the fungal resistance to Ca 2+ , Fe 2+ , and Cr 6+ was noticeable. In the ATR-FTIR analysis, we determined that C-H and C = O were the major functional groups affected by the presence of Cu 2+ , Mn 2+ , and Fe 2+ for L. elongata and in the presence of Cu 2+ and Ca 2+ for B. eronia . It is noteworthy that the highest concentration of Pb 2+ led to the loss of endobacteria in both L. elongata and B. eronia , while the other metals generally increased the concentration of endosymbionts inside the fungal mycelium. From these results, we concluded that bacterial endosymbionts of fungi can play a fundamental role in fungal resistance to metals. This study provides the first step toward a greater understanding of symbiotic interactions between bacteria and fungi in relation to metal tolerance and remediation.« less

Authors:
; ; ;
Publication Date:
Research Org.:
Michigan State Univ., East Lansing, MI (United States). MSU-DOE Plant Research Laboratory
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER); Welch Foundation; National Science Foundation (NSF)
OSTI Identifier:
1908034
Alternate Identifier(s):
OSTI ID: 1903885
Grant/Contract Number:  
LANLF59T; E-2011-20190330; 2125480/2125104/2125298
Resource Type:
Published Article
Journal Name:
Frontiers in Microbiology
Additional Journal Information:
Journal Name: Frontiers in Microbiology Journal Volume: 13; Journal ID: ISSN 1664-302X
Publisher:
Frontiers Media SA
Country of Publication:
Switzerland
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Microbiology; endobacteria; heavy metals; fungi; metal removal; adsorption; host resistance

Citation Formats

Lupini, Simone, Peña-Bahamonde, Janire, Bonito, Gregory, and Rodrigues, Debora F. Effect of Endosymbiotic Bacteria on Fungal Resistance Toward Heavy Metals. Switzerland: N. p., 2022. Web. doi:10.3389/fmicb.2022.822541.
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Lupini, Simone, Peña-Bahamonde, Janire, Bonito, Gregory, & Rodrigues, Debora F. Effect of Endosymbiotic Bacteria on Fungal Resistance Toward Heavy Metals. Switzerland. https://doi.org/10.3389/fmicb.2022.822541
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Lupini, Simone, Peña-Bahamonde, Janire, Bonito, Gregory, and Rodrigues, Debora F. Tue . "Effect of Endosymbiotic Bacteria on Fungal Resistance Toward Heavy Metals". Switzerland. https://doi.org/10.3389/fmicb.2022.822541.
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@article{osti_1908034,
title = {Effect of Endosymbiotic Bacteria on Fungal Resistance Toward Heavy Metals},
author = {Lupini, Simone and Peña-Bahamonde, Janire and Bonito, Gregory and Rodrigues, Debora F.},
abstractNote = {Most studies on metal removal or tolerance by fungi or bacteria focus on single isolates, without taking into consideration that some fungi in nature may be colonized by endobacteria. To address this knowledge gap, we investigated the tolerance and removal of diverse metals with two fungal species: Linnemannia elongata containing Burkholderia-related endobacteria and Benniella erionia containing Mollicute-related endobacteria. Isogenic lines of both species were generated with antibiotic treatments to remove their respective endobacteria. Experiments involved comparing the isogenic lines and wild type fungi in relation to the minimum inhibitory concentration for the metals, the fungal ability to remove these different metals via atomic adsorption spectroscopy, and the interaction of the metals with specific functional groups of the fungi and fungi-bacteria to determine the role of the bacteria via attenuated total reflection fourier transformed infrared (ATR-FTIR). Finally, we determined the influence of different metal concentrations, associated with moderate and high fungal growth inhibition, on the presence of the endobacteria inside the fungal mycelium via quantitative real-time PCR. Results showed that the presence of the endosymbiont increased B. erionia resistance to Mn 2+ and increased the removal of Fe 2+ compared to isogenic lines. The absence of the endosymbiont in L. elongata increased the fungal resistance toward Fe 2+ and improved the removal of Fe 2+ . Furthermore, when the bacterial endosymbiont was present in L. elongata , a decrease in the fungal resistance to Ca 2+ , Fe 2+ , and Cr 6+ was noticeable. In the ATR-FTIR analysis, we determined that C-H and C = O were the major functional groups affected by the presence of Cu 2+ , Mn 2+ , and Fe 2+ for L. elongata and in the presence of Cu 2+ and Ca 2+ for B. eronia . It is noteworthy that the highest concentration of Pb 2+ led to the loss of endobacteria in both L. elongata and B. eronia , while the other metals generally increased the concentration of endosymbionts inside the fungal mycelium. From these results, we concluded that bacterial endosymbionts of fungi can play a fundamental role in fungal resistance to metals. This study provides the first step toward a greater understanding of symbiotic interactions between bacteria and fungi in relation to metal tolerance and remediation.},
doi = {10.3389/fmicb.2022.822541},
journal = {Frontiers in Microbiology},
number = ,
volume = 13,
place = {Switzerland},
year = {Tue Mar 15 00:00:00 EDT 2022},
month = {Tue Mar 15 00:00:00 EDT 2022}
}
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https://doi.org/10.3389/fmicb.2022.822541
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