The Cacti Microbiome: Interplay between Habitat-Filtering and Host-Specificity

Fonseca-García, Citlali; Coleman-Derr, Devin; Garrido, Etzel; Visel, Axel; Tringe, Susannah G.; Partida-Martínez, Laila P.

doi:10.3389/fmicb.2016.00150

Title: The Cacti Microbiome: Interplay between Habitat-Filtering and Host-Specificity

Journal Article · Fri Feb 12 00:00:00 EST 2016 · Frontiers in Microbiology

DOI:https://doi.org/10.3389/fmicb.2016.00150· OSTI ID:1379089

Fonseca-García, Citlali ^[1]; Coleman-Derr, Devin ^[2]; Garrido, Etzel ^[1]; Visel, Axel ^[3]; Tringe, Susannah G. ^[3]; Partida-Martínez, Laila P. ^[1]

Center for Research and Advanced Studies of the National Polytechnic Inst., Irapuato (Mexico). Dept. of Genetic Engineering
USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Environmental Genomics and Systems Biology Division; US Dept. of Agriculture (USDA) Agricultural Research Service, Albany, CA (United States)
USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Environmental Genomics and Systems Biology Division; Univ. of California, Merced, CA (United States). School of Natural Sciences

Cactaceae represents one of the most species-rich families of succulent plants native to arid and semi-arid ecosystems, yet the associations Cacti establish with microorganisms and the rules governing microbial community assembly remain poorly understood. We analyzed the composition, diversity, and factors influencing above- and below-ground bacterial, archaeal, and fungal communities associated with two native and sympatric Cacti species: Myrtillocactus geometrizans and Opuntia robusta. Phylogenetic profiling showed that the composition and assembly of microbial communities associated with Cacti were primarily influenced by the plant compartment; plant species, site, and season played only a minor role. Remarkably, bacterial, and archaeal diversity was higher in the phyllosphere than in the rhizosphere of Cacti, while the opposite was true for fungi. Semi-arid soils exhibited the highest levels of microbial diversity whereas the stem endosphere the lowest. Despite their taxonomic distance, M. geometrizans and O. robusta shared most microbial taxa in all analyzed compartments. Influence of the plant host did only play a larger role in the fungal communities of the stem endosphere. These results suggest that fungi establish specific interactions with their host plant inside the stem, whereas microbial communities in the other plant compartments may play similar functional roles in these two species. Biochemical and molecular characterization of seed-borne bacteria of Cacti supports the idea that these microbial symbionts may be vertically inherited and could promote plant growth and drought tolerance for the fitness of the Cacti holobiont. We envision this knowledge will help improve and sustain agriculture in arid and semi-arid regions of the world.

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Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1379089

Journal Information:: Frontiers in Microbiology, Vol. 7, Issue FEB; ISSN 1664-302X

Publisher:: Frontiers Research FoundationCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 133 works

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The role of inoculum dispersal and plant species identity in the assembly of leaf endophytic fungal communities Ricks, Kevin D.; Koide, Roger T. PLOS ONE, Vol. 14, Issue 7 https://doi.org/10.1371/journal.pone.0219832	journal	July 2019
Effect of aridity and dune type on rhizosphere soil bacterial communities of Caragana microphylla in desert regions of northern China Gao, Jiangli; Luo, Yang; Wei, Yali PLOS ONE, Vol. 14, Issue 10 https://doi.org/10.1371/journal.pone.0224195	journal	October 2019
Fungal-Bacterial Networks in the Populus Rhizobiome Are Impacted by Soil Properties and Host Genotype Bonito, Gregory; Benucci, Gian Maria Niccolò; Hameed, Khalid Frontiers in Microbiology, Vol. 10 https://doi.org/10.3389/fmicb.2019.00481	journal	March 2019
Conservation of Endophyte Bacterial Community Structure Across Two Panicum Grass Species Singer, Esther; Bonnette, Jason; Woyke, Tanja Frontiers in Microbiology, Vol. 10 https://doi.org/10.3389/fmicb.2019.02181	journal	September 2019
Bioprospecting of South African Plants as a Unique Resource for Bioactive Endophytic Microbes Abdalla, Muna Ali; McGaw, Lyndy J. Frontiers in Pharmacology, Vol. 9 https://doi.org/10.3389/fphar.2018.00456	journal	May 2018
Drought Stress and Root-Associated Bacterial Communities Naylor, Dan; Coleman-Derr, Devin Frontiers in Plant Science, Vol. 8 https://doi.org/10.3389/fpls.2017.02223	journal	January 2018
Plant Growth-Promoting Rhizobacteria: Context, Mechanisms of Action, and Roadmap to Commercialization of Biostimulants for Sustainable Agriculture Backer, Rachel; Rokem, J. Stefan; Ilangumaran, Gayathri Frontiers in Plant Science, Vol. 9 https://doi.org/10.3389/fpls.2018.01473	journal	October 2018
Antimicrobial peptide expression in a wild tobacco plant reveals the limits of host-microbe-manipulations in the field Weinhold, Arne; Karimi Dorcheh, Elham; Li, Ran eLife, Vol. 7 https://doi.org/10.7554/elife.28715	journal	April 2018
Ecophylogeny of the endospheric root fungal microbiome of co-occurring Agrostis stolonifera Lê Van, Amandine; Quaiser, Achim; Duhamel, Marie PeerJ, Vol. 5 https://doi.org/10.7717/peerj.3454	journal	January 2017
Biotic filtering of endophytic fungal communities in Bromus tectorum Ricks, Kevin D.; Koide, Roger T. Oecologia, Vol. 189, Issue 4 https://doi.org/10.1007/s00442-019-04388-y	journal	March 2019
Species-wide Metabolic Interaction Network for Understanding Natural Lignocellulose Digestion in Termite Gut Microbiota Kundu, Pritam; Manna, Bharat; Majumder, Subham Scientific Reports, Vol. 9, Issue 1 https://doi.org/10.1038/s41598-019-52843-w	journal	November 2019
Host identity and symbiotic association affects the taxonomic and functional diversity of the clownfish-hosting sea anemone microbiome Titus, Benjamin M.; Laroche, Robert; Rodríguez, Estefanía Biology Letters, Vol. 16, Issue 2 https://doi.org/10.1098/rsbl.2019.0738	journal	February 2020
Rootstocks Shape the Rhizobiome: Rhizosphere and Endosphere Bacterial Communities in the Grafted Tomato System Poudel, Ravin; Jumpponen, Ari; Kennelly, Megan M. Applied and Environmental Microbiology, Vol. 85, Issue 2 https://doi.org/10.1128/aem.01765-18	journal	November 2018
Structural variability and niche differentiation in the rhizosphere and endosphere bacterial microbiome of field-grown poplar trees Beckers, Bram; Op De Beeck, Michiel; Weyens, Nele Microbiome, Vol. 5, Issue 1 https://doi.org/10.1186/s40168-017-0241-2	journal	February 2017
Microbiome Dynamics Associated With the Atacama Flowering Desert Araya, Juan Pablo; González, Máximo; Cardinale, Massimiliano Frontiers in Microbiology, Vol. 10 https://doi.org/10.3389/fmicb.2019.03160	journal	January 2020
Consistent host and organ occupancy of phyllosphere bacteria in a community of wild herbaceous plant species Massoni, Julien; Bortfeld-Miller, Miriam; Jardillier, Ludwig ETH Zurich https://doi.org/10.3929/ethz-b-000387304	text	January 2020
Native and invading yellow starthistle (Centaurea solstitialis) microbiomes differ in composition and diversity of bacteria Lu-Irving, Patricia; Harenčár, Julia; Sounart, Hailey https://doi.org/10.1101/119917	posted_content	August 2018
Unlocking a high bacterial diversity in the coralloid root microbiome from the cycad genus Dioon Suarez-Moo, Pablo de Jesus; Vovides, Andrew P.; Griffith, M. Patrick PLOS ONE https://doi.org/10.1101/381798	journal	August 2018
Consistent host and organ occupancy of phyllosphere bacteria in a community of wild herbaceous plant species Massoni, Julien; Bortfeld-Miller, Miriam; Jardillier, Ludwig The ISME Journal, Vol. 14, Issue 1 https://doi.org/10.1038/s41396-019-0531-8	journal	October 2019
Antimicrobial peptide expression in a wild tobacco plant reveals the limits of host-microbe-manipulations in the field Weinhold, Arne; Dorcheh, Elham Karimi; Li, Ran Freie Universität Berlin https://doi.org/10.17169/refubium-2884	text	January 2019
Fungal community assemblages in a high elevation desert environment: Absence of dispersal limitation and edaphic effects in surface soil Yang, Teng; Adams, Jonathan M.; Shi, Yu Soil Biology and Biochemistry, Vol. 115 https://doi.org/10.1016/j.soilbio.2017.09.013	journal	December 2017
Bacterial Diversity and Population Dynamics During the Fermentation of Palm Wine From Guerrero Mexico Astudillo-Melgar, Fernando; Ochoa-Leyva, Adrián; Utrilla, José Frontiers in Microbiology, Vol. 10 https://doi.org/10.3389/fmicb.2019.00531	journal	March 2019
Endophytic Communities of Transgenic Poplar Were Determined by the Environment and Niche Rather Than by Transgenic Events Wang, Yanbo; Zhang, Weixi; Ding, Changjun Frontiers in Microbiology, Vol. 10 https://doi.org/10.3389/fmicb.2019.00588	journal	March 2019
Functional Signatures of the Epiphytic Prokaryotic Microbiome of Agaves and Cacti Flores-Núñez, Víctor M.; Fonseca-García, Citlali; Desgarennes, Damaris Frontiers in Microbiology, Vol. 10 https://doi.org/10.3389/fmicb.2019.03044	journal	January 2020
Harnessing Host-Vector Microbiome for Sustainable Plant Disease Management of Phloem-Limited Bacteria Trivedi, Pankaj; Trivedi, Chanda; Grinyer, Jasmine Frontiers in Plant Science, Vol. 7 https://doi.org/10.3389/fpls.2016.01423	journal	September 2016
Pumpkin powdery mildew disease severity influences the fungal diversity of the phyllosphere Zhang, Zhuo; Luo, Luyun; Tan, Xinqiu PeerJ Preprints https://doi.org/10.7287/peerj.preprints.3278v1	journal	September 2017
Plant host and drought shape the root associated fungal microbiota in rice Andreo-Jimenez, Beatriz; Vandenkoornhuyse, Philippe; Lê Van, Amandine PeerJ, Vol. 7 https://doi.org/10.7717/peerj.7463	journal	January 2019

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