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Title: Functional Signatures of the Epiphytic Prokaryotic Microbiome of Agaves and Cacti

Abstract

Microbial symbionts account for survival, development, fitness and evolution of eukaryotic hosts. These microorganisms together with their host form a biological unit known as holobiont. Recent studies have revealed that the holobiont of agaves and cacti comprises a diverse and structured microbiome, which might be important for its adaptation to drylands. Here, we investigated the functional signatures of the prokaryotic communities of the soil and the episphere, that includes the rhizosphere and phyllosphere, associated with the cultivated Agave tequilana and the native and sympatric Agave salmiana, Opuntia robusta and Myrtillocactus geometrizans by mining shotgun metagenomic data. Consistent with previous phylogenetic profiling, we found that Proteobacteria, Actinobacteria and Firmicutes were the main represented phyla in the episphere of agaves and cacti, and that clustering of metagenomes correlated with the plant compartment. In native plants, genes related to aerobic anoxygenic phototrophy and photosynthesis were enriched in the phyllosphere and soil, while genes coding for biofilm formation and quorum sensing were enriched in both epiphytic communities. In the episphere of cultivated A. tequilana fewer genes were identified, but they belonged to similar pathways than those found in native plants. A. tequilana showed a depletion in several genes belonging to carbon metabolism, secondary metabolitemore » biosynthesis and xenobiotic degradation suggesting that its lower microbial diversity might be linked to functional losses. However, this species also showed an enrichment in biofilm and quorum sensing in the epiphytic compartments, and evidence for nitrogen fixation in the rhizosphere. Aerobic anoxygenic phototrophic markers were represented by Rhizobiales (Methylobacterium) and Rhodospirillales (Belnapia) in the phyllosphere, while photosystem genes were widespread in Bacillales and Cyanobacteria. Nitrogen fixation and biofilm formation genes were mostly related to Proteobacteria. These analyses support the idea of niche differentiation in the rhizosphere and phyllosphere of agaves and cacti and shed light on the potential mechanisms by which epiphytic microbial communities survive and colonize plants of arid and semiarid ecosystems. This study establishes a guideline for testing the relevance of the identified functional traits on the microbial community and the plant fitness.« less

Authors:
; ; ; ; ;
Publication Date:
Research Org.:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC); Consejo Nacional de Ciencia y Tecnología in Mexico (CONACyT)
OSTI Identifier:
1592177
Alternate Identifier(s):
OSTI ID: 1604667
Grant/Contract Number:  
AC02-05CH11231; CB-2010-01-151007; INFR-2012-01-197799; FOINS-2015-01-006; A1-S-9889
Resource Type:
Published Article
Journal Name:
Frontiers in Microbiology
Additional Journal Information:
Journal Name: Frontiers in Microbiology Journal Volume: 10; Journal ID: ISSN 1664-302X
Publisher:
Frontiers Research Foundation
Country of Publication:
Switzerland
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; arid and semiarid environments; metagenomics; phyllosphere; rhizosphere; soil; CAM plants; phototrophy

Citation Formats

Flores-Núñez, Víctor M., Fonseca-García, Citlali, Desgarennes, Damaris, Eloe-Fadrosh, Emiley, Woyke, Tanja, and Partida-Martínez, Laila P. Functional Signatures of the Epiphytic Prokaryotic Microbiome of Agaves and Cacti. Switzerland: N. p., 2020. Web. doi:10.3389/fmicb.2019.03044.
Flores-Núñez, Víctor M., Fonseca-García, Citlali, Desgarennes, Damaris, Eloe-Fadrosh, Emiley, Woyke, Tanja, & Partida-Martínez, Laila P. Functional Signatures of the Epiphytic Prokaryotic Microbiome of Agaves and Cacti. Switzerland. doi:10.3389/fmicb.2019.03044.
Flores-Núñez, Víctor M., Fonseca-García, Citlali, Desgarennes, Damaris, Eloe-Fadrosh, Emiley, Woyke, Tanja, and Partida-Martínez, Laila P. Fri . "Functional Signatures of the Epiphytic Prokaryotic Microbiome of Agaves and Cacti". Switzerland. doi:10.3389/fmicb.2019.03044.
@article{osti_1592177,
title = {Functional Signatures of the Epiphytic Prokaryotic Microbiome of Agaves and Cacti},
author = {Flores-Núñez, Víctor M. and Fonseca-García, Citlali and Desgarennes, Damaris and Eloe-Fadrosh, Emiley and Woyke, Tanja and Partida-Martínez, Laila P.},
abstractNote = {Microbial symbionts account for survival, development, fitness and evolution of eukaryotic hosts. These microorganisms together with their host form a biological unit known as holobiont. Recent studies have revealed that the holobiont of agaves and cacti comprises a diverse and structured microbiome, which might be important for its adaptation to drylands. Here, we investigated the functional signatures of the prokaryotic communities of the soil and the episphere, that includes the rhizosphere and phyllosphere, associated with the cultivated Agave tequilana and the native and sympatric Agave salmiana, Opuntia robusta and Myrtillocactus geometrizans by mining shotgun metagenomic data. Consistent with previous phylogenetic profiling, we found that Proteobacteria, Actinobacteria and Firmicutes were the main represented phyla in the episphere of agaves and cacti, and that clustering of metagenomes correlated with the plant compartment. In native plants, genes related to aerobic anoxygenic phototrophy and photosynthesis were enriched in the phyllosphere and soil, while genes coding for biofilm formation and quorum sensing were enriched in both epiphytic communities. In the episphere of cultivated A. tequilana fewer genes were identified, but they belonged to similar pathways than those found in native plants. A. tequilana showed a depletion in several genes belonging to carbon metabolism, secondary metabolite biosynthesis and xenobiotic degradation suggesting that its lower microbial diversity might be linked to functional losses. However, this species also showed an enrichment in biofilm and quorum sensing in the epiphytic compartments, and evidence for nitrogen fixation in the rhizosphere. Aerobic anoxygenic phototrophic markers were represented by Rhizobiales (Methylobacterium) and Rhodospirillales (Belnapia) in the phyllosphere, while photosystem genes were widespread in Bacillales and Cyanobacteria. Nitrogen fixation and biofilm formation genes were mostly related to Proteobacteria. These analyses support the idea of niche differentiation in the rhizosphere and phyllosphere of agaves and cacti and shed light on the potential mechanisms by which epiphytic microbial communities survive and colonize plants of arid and semiarid ecosystems. This study establishes a guideline for testing the relevance of the identified functional traits on the microbial community and the plant fitness.},
doi = {10.3389/fmicb.2019.03044},
journal = {Frontiers in Microbiology},
number = ,
volume = 10,
place = {Switzerland},
year = {2020},
month = {1}
}

Journal Article:
Free Publicly Available Full Text
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DOI: 10.3389/fmicb.2019.03044

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