Temporal and Spatial Changes in Phyllosphere Microbiome of Acacia Trees Growing in Arid Environments

Background: The evolutionary relationships between plants and their microbiomes are of high importance to the survival of plants in general and even more in extreme conditions. Changes in the plant's microbiome can affect plant development, growth, fitness, and health. Along the arid Arava, sou...

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Main Authors: Ashraf Al Ashhab, Shiri Meshner, Rivka Alexander-Shani, Hana Dimerets, Michael Brandwein, Yael Bar-Lavan, Gidon Winters
Format: Article
Language:English
Published: Frontiers Media S.A. 2021-07-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2021.656269/full
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author Ashraf Al Ashhab
Ashraf Al Ashhab
Shiri Meshner
Rivka Alexander-Shani
Hana Dimerets
Michael Brandwein
Michael Brandwein
Yael Bar-Lavan
Gidon Winters
Gidon Winters
author_facet Ashraf Al Ashhab
Ashraf Al Ashhab
Shiri Meshner
Rivka Alexander-Shani
Hana Dimerets
Michael Brandwein
Michael Brandwein
Yael Bar-Lavan
Gidon Winters
Gidon Winters
author_sort Ashraf Al Ashhab
collection DOAJ
description Background: The evolutionary relationships between plants and their microbiomes are of high importance to the survival of plants in general and even more in extreme conditions. Changes in the plant's microbiome can affect plant development, growth, fitness, and health. Along the arid Arava, southern Israel, acacia trees (Acacia raddiana and Acacia tortilis) are considered keystone species. In this study, we investigated the ecological effects of plant species, microclimate, phenology, and seasonality on the epiphytic and endophytic microbiome of acacia trees. One hundred thirty-nine leaf samples were collected throughout the sampling year and were assessed using 16S rDNA gene amplified with five different primers (targeting different gene regions) and sequenced (150 bp paired-end) on an Illumina MiSeq sequencing platform.Results: Epiphytic bacterial diversity indices (Shannon–Wiener, Chao1, Simpson, and observed number of operational taxonomic units) were found to be nearly double compared to endophyte counterparts. Epiphyte and endophyte communities were significantly different from each other in terms of the composition of the microbial associations. Interestingly, the epiphytic bacterial diversity was similar in the two acacia species, but the canopy sides and sample months exhibited different diversity, whereas the endophytic bacterial communities were different in the two acacia species but similar throughout the year. Abiotic factors, such as air temperature and precipitation, were shown to significantly affect both epiphyte and endophytes communities. Bacterial community compositions showed that Firmicutes dominate A. raddiana, and Proteobacteria dominate A. tortilis; these bacterial communities consisted of only a small number of bacterial families, mainly Bacillaceae and Comamonadaceae in the endophyte for A. raddiana and A. tortilis, respectively, and Geodematophilaceae and Micrococcaceae for epiphyte bacterial communities, respectively. Interestingly, ~60% of the obtained bacterial classifications were unclassified below family level (i.e., “new”).Conclusions: These results shed light on the unique desert phyllosphere microbiome highlighting the importance of multiple genotypic and abiotic factors in shaping the epiphytic and endophytic microbial communities. This study also shows that only a few bacterial families dominate both epiphyte and endophyte communities, highlighting the importance of climate change (precipitation, air temperature, and humidity) in affecting arid land ecosystems where acacia trees are considered keystone species.
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spelling doaj.art-09e347d4497c46e4b6a0b316e128a5d12022-12-21T22:41:03ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2021-07-011210.3389/fmicb.2021.656269656269Temporal and Spatial Changes in Phyllosphere Microbiome of Acacia Trees Growing in Arid EnvironmentsAshraf Al Ashhab0Ashraf Al Ashhab1Shiri Meshner2Rivka Alexander-Shani3Hana Dimerets4Michael Brandwein5Michael Brandwein6Yael Bar-Lavan7Gidon Winters8Gidon Winters9Dead Sea and Arava Science Center, Masada, IsraelBen-Gurion University of the Negev, Eilat Campus, Be'er Sheva, IsraelDead Sea and Arava Science Center, Masada, IsraelDead Sea and Arava Science Center, Masada, IsraelDead Sea and Arava Science Center, Masada, IsraelDead Sea and Arava Science Center, Masada, IsraelBiofilm Research Laboratory, Faculty of Dental Medicine, Hebrew University of Jerusalem, Jerusalem, IsraelDead Sea and Arava Science Center, Masada, IsraelDead Sea and Arava Science Center, Masada, IsraelBen-Gurion University of the Negev, Eilat Campus, Be'er Sheva, IsraelBackground: The evolutionary relationships between plants and their microbiomes are of high importance to the survival of plants in general and even more in extreme conditions. Changes in the plant's microbiome can affect plant development, growth, fitness, and health. Along the arid Arava, southern Israel, acacia trees (Acacia raddiana and Acacia tortilis) are considered keystone species. In this study, we investigated the ecological effects of plant species, microclimate, phenology, and seasonality on the epiphytic and endophytic microbiome of acacia trees. One hundred thirty-nine leaf samples were collected throughout the sampling year and were assessed using 16S rDNA gene amplified with five different primers (targeting different gene regions) and sequenced (150 bp paired-end) on an Illumina MiSeq sequencing platform.Results: Epiphytic bacterial diversity indices (Shannon–Wiener, Chao1, Simpson, and observed number of operational taxonomic units) were found to be nearly double compared to endophyte counterparts. Epiphyte and endophyte communities were significantly different from each other in terms of the composition of the microbial associations. Interestingly, the epiphytic bacterial diversity was similar in the two acacia species, but the canopy sides and sample months exhibited different diversity, whereas the endophytic bacterial communities were different in the two acacia species but similar throughout the year. Abiotic factors, such as air temperature and precipitation, were shown to significantly affect both epiphyte and endophytes communities. Bacterial community compositions showed that Firmicutes dominate A. raddiana, and Proteobacteria dominate A. tortilis; these bacterial communities consisted of only a small number of bacterial families, mainly Bacillaceae and Comamonadaceae in the endophyte for A. raddiana and A. tortilis, respectively, and Geodematophilaceae and Micrococcaceae for epiphyte bacterial communities, respectively. Interestingly, ~60% of the obtained bacterial classifications were unclassified below family level (i.e., “new”).Conclusions: These results shed light on the unique desert phyllosphere microbiome highlighting the importance of multiple genotypic and abiotic factors in shaping the epiphytic and endophytic microbial communities. This study also shows that only a few bacterial families dominate both epiphyte and endophyte communities, highlighting the importance of climate change (precipitation, air temperature, and humidity) in affecting arid land ecosystems where acacia trees are considered keystone species.https://www.frontiersin.org/articles/10.3389/fmicb.2021.656269/fullAcacia raddianaAcacia tortilisphyllospheredesert plantsmicrobiomeendophytes
spellingShingle Ashraf Al Ashhab
Ashraf Al Ashhab
Shiri Meshner
Rivka Alexander-Shani
Hana Dimerets
Michael Brandwein
Michael Brandwein
Yael Bar-Lavan
Gidon Winters
Gidon Winters
Temporal and Spatial Changes in Phyllosphere Microbiome of Acacia Trees Growing in Arid Environments
Frontiers in Microbiology
Acacia raddiana
Acacia tortilis
phyllosphere
desert plants
microbiome
endophytes
title Temporal and Spatial Changes in Phyllosphere Microbiome of Acacia Trees Growing in Arid Environments
title_full Temporal and Spatial Changes in Phyllosphere Microbiome of Acacia Trees Growing in Arid Environments
title_fullStr Temporal and Spatial Changes in Phyllosphere Microbiome of Acacia Trees Growing in Arid Environments
title_full_unstemmed Temporal and Spatial Changes in Phyllosphere Microbiome of Acacia Trees Growing in Arid Environments
title_short Temporal and Spatial Changes in Phyllosphere Microbiome of Acacia Trees Growing in Arid Environments
title_sort temporal and spatial changes in phyllosphere microbiome of acacia trees growing in arid environments
topic Acacia raddiana
Acacia tortilis
phyllosphere
desert plants
microbiome
endophytes
url https://www.frontiersin.org/articles/10.3389/fmicb.2021.656269/full
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