Cargando…

The Role of Hydrophobicity and Surface Receptors at Hyphae of Lyophyllum sp. Strain Karsten in the Interaction with Burkholderia terrae BS001 – Implications for Interactions in Soil

The soil bacterium Burkholderia terrae strain BS001 can interact with varying soil fungi, using mechanisms that range from the utilization of carbon/energy sources such as glycerol to the ability to reach novel territories in soil via co-migration with growing fungal mycelia. Here, we investigate th...

Descripción completa

Detalles Bibliográficos
Autores principales: Vila, Taissa, Nazir, Rashid, Rozental, Sonia, dos Santos, Giulia M. P., Calixto, Renata O. R., Barreto-Bergter, Eliana, Wick, Lukas Y., van Elsas, Jan Dirk
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5081359/
https://www.ncbi.nlm.nih.gov/pubmed/27833591
http://dx.doi.org/10.3389/fmicb.2016.01689
_version_ 1782462874479755264
author Vila, Taissa
Nazir, Rashid
Rozental, Sonia
dos Santos, Giulia M. P.
Calixto, Renata O. R.
Barreto-Bergter, Eliana
Wick, Lukas Y.
van Elsas, Jan Dirk
author_facet Vila, Taissa
Nazir, Rashid
Rozental, Sonia
dos Santos, Giulia M. P.
Calixto, Renata O. R.
Barreto-Bergter, Eliana
Wick, Lukas Y.
van Elsas, Jan Dirk
author_sort Vila, Taissa
collection PubMed
description The soil bacterium Burkholderia terrae strain BS001 can interact with varying soil fungi, using mechanisms that range from the utilization of carbon/energy sources such as glycerol to the ability to reach novel territories in soil via co-migration with growing fungal mycelia. Here, we investigate the intrinsic properties of the B. terrae BS001 interaction with the basidiomycetous soil fungus Lyophyllum sp. strain Karsten. In some experiments, the ascomycetous Trichoderma asperellum 302 was also used. The hyphae of Lyophyllum sp. strain Karsten were largely hydrophilic on water-containing media versus hydrophobic when aerial, as evidenced by contact angle analyses (CA). Co-migration of B. terrae strain BS001 cells with the hyphae of the two fungi occurred preferentially along the - presumably hydrophilic - soil-dwelling hyphae, whereas aerial hyphae did not allow efficient migration, due to reduced thickness of their surrounding mucous films. Moreover, the cell numbers over the length of the hyphae in soil showed an uneven distribution, i.e., the CFU numbers increased from minima at the inoculation point to maximal numbers in the middle of the extended hyphae, then decreasing toward the terminal side. Microscopic analyses of the strain BS001 associations with the Lyophyllum sp. strain Karsten hyphae in the microcosms confirmed the presence of B. terrae BS001 cells on the mucous matter that was present at the hyphal surfaces of the fungi used. Cell agglomerates were found to accumulate at defined sites on the hyphal surfaces, which were coined ‘fungal-interactive’ hot spots. Evidence was further obtained for the contention that receptors for a physical bacterium-fungus interaction occur at the Lyophyllum sp. strain Karsten hyphal surface, in which the specific glycosphingolipid ceramide monohexoside (CMH) plays an important role. Thus, bacterial adherence may be mediated by heterogeneously distributed fungal-specific receptors, implying the CMH moieties. This study sheds light on the physical aspects of the B. terrae BS001 – Lyophyllum sp. strain Karsten interaction, highlighting heterogeneity along the hyphae with respect to hydrophobicity and the presence of potential anchoring sites.
format Online
Article
Text
id pubmed-5081359
institution National Center for Biotechnology Information
language English
publishDate 2016
publisher Frontiers Media S.A.
record_format MEDLINE/PubMed
spelling pubmed-50813592016-11-10 The Role of Hydrophobicity and Surface Receptors at Hyphae of Lyophyllum sp. Strain Karsten in the Interaction with Burkholderia terrae BS001 – Implications for Interactions in Soil Vila, Taissa Nazir, Rashid Rozental, Sonia dos Santos, Giulia M. P. Calixto, Renata O. R. Barreto-Bergter, Eliana Wick, Lukas Y. van Elsas, Jan Dirk Front Microbiol Microbiology The soil bacterium Burkholderia terrae strain BS001 can interact with varying soil fungi, using mechanisms that range from the utilization of carbon/energy sources such as glycerol to the ability to reach novel territories in soil via co-migration with growing fungal mycelia. Here, we investigate the intrinsic properties of the B. terrae BS001 interaction with the basidiomycetous soil fungus Lyophyllum sp. strain Karsten. In some experiments, the ascomycetous Trichoderma asperellum 302 was also used. The hyphae of Lyophyllum sp. strain Karsten were largely hydrophilic on water-containing media versus hydrophobic when aerial, as evidenced by contact angle analyses (CA). Co-migration of B. terrae strain BS001 cells with the hyphae of the two fungi occurred preferentially along the - presumably hydrophilic - soil-dwelling hyphae, whereas aerial hyphae did not allow efficient migration, due to reduced thickness of their surrounding mucous films. Moreover, the cell numbers over the length of the hyphae in soil showed an uneven distribution, i.e., the CFU numbers increased from minima at the inoculation point to maximal numbers in the middle of the extended hyphae, then decreasing toward the terminal side. Microscopic analyses of the strain BS001 associations with the Lyophyllum sp. strain Karsten hyphae in the microcosms confirmed the presence of B. terrae BS001 cells on the mucous matter that was present at the hyphal surfaces of the fungi used. Cell agglomerates were found to accumulate at defined sites on the hyphal surfaces, which were coined ‘fungal-interactive’ hot spots. Evidence was further obtained for the contention that receptors for a physical bacterium-fungus interaction occur at the Lyophyllum sp. strain Karsten hyphal surface, in which the specific glycosphingolipid ceramide monohexoside (CMH) plays an important role. Thus, bacterial adherence may be mediated by heterogeneously distributed fungal-specific receptors, implying the CMH moieties. This study sheds light on the physical aspects of the B. terrae BS001 – Lyophyllum sp. strain Karsten interaction, highlighting heterogeneity along the hyphae with respect to hydrophobicity and the presence of potential anchoring sites. Frontiers Media S.A. 2016-10-27 /pmc/articles/PMC5081359/ /pubmed/27833591 http://dx.doi.org/10.3389/fmicb.2016.01689 Text en Copyright © 2016 Vila, Nazir, Rozental, dos Santos, Calixto, Barreto-Bergter, Wick and van Elsas. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Microbiology
Vila, Taissa
Nazir, Rashid
Rozental, Sonia
dos Santos, Giulia M. P.
Calixto, Renata O. R.
Barreto-Bergter, Eliana
Wick, Lukas Y.
van Elsas, Jan Dirk
The Role of Hydrophobicity and Surface Receptors at Hyphae of Lyophyllum sp. Strain Karsten in the Interaction with Burkholderia terrae BS001 – Implications for Interactions in Soil
title The Role of Hydrophobicity and Surface Receptors at Hyphae of Lyophyllum sp. Strain Karsten in the Interaction with Burkholderia terrae BS001 – Implications for Interactions in Soil
title_full The Role of Hydrophobicity and Surface Receptors at Hyphae of Lyophyllum sp. Strain Karsten in the Interaction with Burkholderia terrae BS001 – Implications for Interactions in Soil
title_fullStr The Role of Hydrophobicity and Surface Receptors at Hyphae of Lyophyllum sp. Strain Karsten in the Interaction with Burkholderia terrae BS001 – Implications for Interactions in Soil
title_full_unstemmed The Role of Hydrophobicity and Surface Receptors at Hyphae of Lyophyllum sp. Strain Karsten in the Interaction with Burkholderia terrae BS001 – Implications for Interactions in Soil
title_short The Role of Hydrophobicity and Surface Receptors at Hyphae of Lyophyllum sp. Strain Karsten in the Interaction with Burkholderia terrae BS001 – Implications for Interactions in Soil
title_sort role of hydrophobicity and surface receptors at hyphae of lyophyllum sp. strain karsten in the interaction with burkholderia terrae bs001 – implications for interactions in soil
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5081359/
https://www.ncbi.nlm.nih.gov/pubmed/27833591
http://dx.doi.org/10.3389/fmicb.2016.01689
work_keys_str_mv AT vilataissa theroleofhydrophobicityandsurfacereceptorsathyphaeoflyophyllumspstrainkarstenintheinteractionwithburkholderiaterraebs001implicationsforinteractionsinsoil
AT nazirrashid theroleofhydrophobicityandsurfacereceptorsathyphaeoflyophyllumspstrainkarstenintheinteractionwithburkholderiaterraebs001implicationsforinteractionsinsoil
AT rozentalsonia theroleofhydrophobicityandsurfacereceptorsathyphaeoflyophyllumspstrainkarstenintheinteractionwithburkholderiaterraebs001implicationsforinteractionsinsoil
AT dossantosgiuliamp theroleofhydrophobicityandsurfacereceptorsathyphaeoflyophyllumspstrainkarstenintheinteractionwithburkholderiaterraebs001implicationsforinteractionsinsoil
AT calixtorenataor theroleofhydrophobicityandsurfacereceptorsathyphaeoflyophyllumspstrainkarstenintheinteractionwithburkholderiaterraebs001implicationsforinteractionsinsoil
AT barretobergtereliana theroleofhydrophobicityandsurfacereceptorsathyphaeoflyophyllumspstrainkarstenintheinteractionwithburkholderiaterraebs001implicationsforinteractionsinsoil
AT wicklukasy theroleofhydrophobicityandsurfacereceptorsathyphaeoflyophyllumspstrainkarstenintheinteractionwithburkholderiaterraebs001implicationsforinteractionsinsoil
AT vanelsasjandirk theroleofhydrophobicityandsurfacereceptorsathyphaeoflyophyllumspstrainkarstenintheinteractionwithburkholderiaterraebs001implicationsforinteractionsinsoil
AT vilataissa roleofhydrophobicityandsurfacereceptorsathyphaeoflyophyllumspstrainkarstenintheinteractionwithburkholderiaterraebs001implicationsforinteractionsinsoil
AT nazirrashid roleofhydrophobicityandsurfacereceptorsathyphaeoflyophyllumspstrainkarstenintheinteractionwithburkholderiaterraebs001implicationsforinteractionsinsoil
AT rozentalsonia roleofhydrophobicityandsurfacereceptorsathyphaeoflyophyllumspstrainkarstenintheinteractionwithburkholderiaterraebs001implicationsforinteractionsinsoil
AT dossantosgiuliamp roleofhydrophobicityandsurfacereceptorsathyphaeoflyophyllumspstrainkarstenintheinteractionwithburkholderiaterraebs001implicationsforinteractionsinsoil
AT calixtorenataor roleofhydrophobicityandsurfacereceptorsathyphaeoflyophyllumspstrainkarstenintheinteractionwithburkholderiaterraebs001implicationsforinteractionsinsoil
AT barretobergtereliana roleofhydrophobicityandsurfacereceptorsathyphaeoflyophyllumspstrainkarstenintheinteractionwithburkholderiaterraebs001implicationsforinteractionsinsoil
AT wicklukasy roleofhydrophobicityandsurfacereceptorsathyphaeoflyophyllumspstrainkarstenintheinteractionwithburkholderiaterraebs001implicationsforinteractionsinsoil
AT vanelsasjandirk roleofhydrophobicityandsurfacereceptorsathyphaeoflyophyllumspstrainkarstenintheinteractionwithburkholderiaterraebs001implicationsforinteractionsinsoil