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Soil, land care and environmental research
RESEARCH ARTICLE

Perennials but not slope aspect affect the diversity of soil bacterial communities in the northern Negev Desert, Israel

Ahuva Vonshak A , Menachem Y. Sklarz B , Ann M. Hirsch C and Osnat Gillor A D
+ Author Affiliations
- Author Affiliations

A Zuckerberg Institute for Water Research, Blaustein Institutes for Desert Research, Ben-Gurion University of the Negev, Israel.

B Bioinformatics Core Facility, Ben-Gurion University of the Negev, Israel.

C Department of Molecular, Cell and Developmental Biology and Molecular Biology Institute, University of California Los Angeles, Los Angeles, CA, USA.

D Corresponding author. Email: gilloro@bgu.ac.il

Soil Research - https://doi.org/10.1071/SR17010
Submitted: 9 January 2017  Accepted: 25 July 2017   Published online: 18 December 2017

Abstract

Underneath the canopy of perennials in arid regions, moderate soil temperature and evaporation, as well as plant litter create islands of higher fertility in the low-productivity landscape, known as ‘resource islands’. The sparse distribution of these resource islands is mirrored by soil microbial communities, which mediate a large number of biogeochemical transformations underneath the plants. We explored the link between the bacterial community composition and two prevalent desert shrubs, Zygophyllum dumosum and Artemisia herba-alba, on northern- and southern-facing slopes in the northern highlands of the Negev Desert (Israel), at the end of a drought winter mild rainy season. We sequenced the bacterial community and analysed the physicochemical properties of the soil under the shrub canopies and from barren soil in replicate slopes. The soil bacterial diversity was independent of slope aspect, but differed according to shrub presence or type. Links between soil bacterial community composition and their associated desert shrubs were found, enabling us to link bacterial diversity with shrub type or barren soils. Our results suggest that plants and their associated bacterial communities are connected to survival and persistence under the harsh desert conditions.

Additional keywords: 16S rRNA, desert plants, next generation sequencing, ecosystem engineer, fertility island.


References

Aguilera LE, Armas C, Cea AP, Gutiérrez JR, Meserve PL, Kelt DA (2016) Rainfall, microhabitat, and small mammals influence the abundance and distribution of soil microorganisms in a Chilean semi-arid shrubland. Journal of Arid Environments 126, 37–46.
Rainfall, microhabitat, and small mammals influence the abundance and distribution of soil microorganisms in a Chilean semi-arid shrubland.CrossRef |

Angel R, Conrad R (2009) In situ measurement of methane fluxes and analysis of transcribed particulate methane monooxygenase in desert soils. Environmental Microbiology 11, 2598–2610.
In situ measurement of methane fluxes and analysis of transcribed particulate methane monooxygenase in desert soils.CrossRef | 1:CAS:528:DC%2BD1MXhtlKisLrP&md5=1e80ce4ed5656446621b78d0a24e13c5CAS |

Bachar A, Soares MI, Gillor O (2012) The effect of resource islands on abundance and diversity of bacteria in arid soils. Microbial Ecology 63, 694–700.
The effect of resource islands on abundance and diversity of bacteria in arid soils.CrossRef |

Bashan Y, de-Bashan LE (2010) Microbial populations of arid lands and their potential for restoration of deserts. In ‘Soil biology and agriculture in the tropics’. (Ed. P Dion). pp. 109–137. (Springer: Berlin, Heidelberg, Germany)

Berg N, Unc A, Steinberger Y (2015) Examination of biotic and abiotic controls of soil bacterial diversity under perennial shrubs in xeric soils. Catena 127, 124–128.
Examination of biotic and abiotic controls of soil bacterial diversity under perennial shrubs in xeric soils.CrossRef |

Bowker MA, Belnap J, Davidson DW, Goldstein H (2006) Correlates of biological soil crust abundance across a continuum of spatial scales: support for a hierarchical conceptual model: Scale-dependent soil crust distribution. Journal of Applied Ecology 43, 152–163.
Correlates of biological soil crust abundance across a continuum of spatial scales: support for a hierarchical conceptual model: Scale-dependent soil crust distribution.CrossRef |

Camargo-Ricalde SL, Dhillion SS (2003) Endemic Mimosa species can serve as mycorrhizal ‘resource islands’ within semiarid communities of the Tehuacán-Cuicatlán Valley, Mexico. Mycorrhiza 13, 129–136.
Endemic Mimosa species can serve as mycorrhizal ‘resource islands’ within semiarid communities of the Tehuacán-Cuicatlán Valley, Mexico.CrossRef |

Caporaso JG, Bittinger K, Bushman FD, DeSantis TZ, Andersen GL, Knight R (2010) PyNAST: a flexible tool for aligning sequences to a template alignment. Bioinformatics 26, 266–267.
PyNAST: a flexible tool for aligning sequences to a template alignment.CrossRef | 1:CAS:528:DC%2BC3cXntlGqug%3D%3D&md5=795f40b3bc76ec64fc465cd759c77ae1CAS |

Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Lozupone CA, Turnbaugh PJ, Fierer N, Knight R (2011) Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proceedings of the National Academy of Sciences of the United States of America 108, 4516–4522.
Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample.CrossRef | 1:CAS:528:DC%2BC3MXjvVCktL0%3D&md5=77b4bb5cb8eec7a57c17b28633dbe425CAS |

Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Huntley J, Fierer N, Owens SM, Betley J, Fraser L, Bauer M, Gormley N, Gilbert JA, Smith G, Knight R (2012) Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. The ISME Journal 6, 1621–1624.
Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms.CrossRef | 1:CAS:528:DC%2BC38XhtVOjtL3N&md5=a58ea8f0e210c4ef505e5fee3ded96c1CAS |

Carrillo-Garcia A, Bashan Y, Rivera ED, Bethlenfalvay GJ (2000a) Effects of resource-island soils, competition, and inoculation with Azospirillum on survival and growth of Pachycereus pringlei, the giant cactus of the Sonoran Desert. Restoration Ecology 8, 65–73.
Effects of resource-island soils, competition, and inoculation with Azospirillum on survival and growth of Pachycereus pringlei, the giant cactus of the Sonoran Desert.CrossRef |

Carrillo-Garcia A, Bashan Y, Bethlenfalvay GJ (2000b) Resource-island soils and the survival of the giant cactus, cardon, of Baja California Sur. Plant and Soil 218, 207–214.
Resource-island soils and the survival of the giant cactus, cardon, of Baja California Sur.CrossRef | 1:CAS:528:DC%2BD3cXhvVGrtb0%3D&md5=2abc7ec02b0e4ac05eab42a9bfea1f0cCAS |

DeSantis TZ, Hugenholtz P, Larsen N, Rojas M, Brodie EL, Keller K, Huber T, Dalevi D, Hu P, Andersen GL (2006) Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Applied and Environmental Microbiology 72, 5069–5072.
Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB.CrossRef | 1:CAS:528:DC%2BD28XnsVaqtLg%3D&md5=50892d99e097fa9ee48e685865295f7dCAS |

Drezner TD, Lazarus BL (2008) The population dynamics of columnar and other cacti: a review. Geography Compass 2, 1–29.
The population dynamics of columnar and other cacti: a review.CrossRef |

Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26, 2460–2461.
Search and clustering orders of magnitude faster than BLAST.CrossRef | 1:CAS:528:DC%2BC3cXht1WhtbzM&md5=050b3d6862b60dccb80d98e0b30cd2a1CAS |

Friedman J (1971) The effect of competition by adult Zygophyllum dumosum Boiss. on seedlings of Artemisia herba-alba Asso in the Negev Desert of Israel. Journal of Ecology 59, 775
The effect of competition by adult Zygophyllum dumosum Boiss. on seedlings of Artemisia herba-alba Asso in the Negev Desert of Israel.CrossRef |

Friedman J, Orshan G, Ziger-Cfir Y (1977) Suppression of annuals by Artemisia herba-alba in the Negev Desert of Israel. Journal of Ecology 65, 413
Suppression of annuals by Artemisia herba-alba in the Negev Desert of Israel.CrossRef |

Granot G, Sikron-Persi N, Gaspan O, Florentin A, Talwara S, Paul LK, Morgenstern Y, Granot Y, Grafi G (2009) Histone modifications associated with drought tolerance in the desert plant Zygophyllum dumosum Boiss. Planta 231, 27–34.
Histone modifications associated with drought tolerance in the desert plant Zygophyllum dumosum Boiss.CrossRef | 1:CAS:528:DC%2BD1MXhsValu7bI&md5=49ad40779de7118ff01e9c7f0379c4a0CAS |

Haas BJ, Gevers D, Earl AM, Feldgarden M, Ward DV, Giannoukos G, Ciulla D, Tabbaa D, Highlander SK, Sodergren E, Methe B, DeSantis TZ, The Human Microbiome Consortium Petrosino JF, Knight R, Birren BW (2011) Chimeric 16S rRNA sequence formation and detection in Sanger and 454-pyrosequenced PCR amplicons. Genome Research 21, 494–504.
Chimeric 16S rRNA sequence formation and detection in Sanger and 454-pyrosequenced PCR amplicons.CrossRef | 1:CAS:528:DC%2BC3MXjt1aisbc%3D&md5=1d46b2f9708f641ae0370e22c824ddb1CAS |

Harlev E, Nevo E, Mirsky N, Ofir R (2013) Antidiabetic attributes of desert and steppic plants: a review. Planta Medica 79, 425–436.
Antidiabetic attributes of desert and steppic plants: a review.CrossRef | 1:CAS:528:DC%2BC3sXpslyqu7s%3D&md5=6d94cb031264342198fb724d62be20c5CAS |

Herman RP, Provencio KR, Herrera-Matos J, Torrez RJ (1995) Resource islands predict the distribution of heterotrophic bacteria in Chihuahuan Desert soils. Applied and Environmental Microbiology 61, 1816–1821.

Iii THN, White SL, Marsh JE (1977) Lichen and moss distribution and biomass in hot desert ecosystems. The Bryologist 80, 470
Lichen and moss distribution and biomass in hot desert ecosystems.CrossRef |

Kaplan D, Maymon M, Agapakis CM, Lee A, Wang A, Prigge BA, Volkogon M, Hirsch AM (2013) A survey of the microbial community in the rhizosphere of two dominant shrubs of the Negev Desert highlands, Zygophyllum dumosum (Zygophyllaceae) and Atriplex halimus (Amaranthaceae), using cultivation-dependent and cultivation-independent methods. American Journal of Botany 100, 1713–1725.
A survey of the microbial community in the rhizosphere of two dominant shrubs of the Negev Desert highlands, Zygophyllum dumosum (Zygophyllaceae) and Atriplex halimus (Amaranthaceae), using cultivation-dependent and cultivation-independent methods.CrossRef |

Klindworth A, Pruesse E, Schweer T, Peplies J, Quast C, Horn M, Glockner FO (2013) Evaluation of general 16S ribosomal RNA gene PCR primers for classical and next-generation sequencing-based diversity studies. Nucleic Acids Research 41, e1
Evaluation of general 16S ribosomal RNA gene PCR primers for classical and next-generation sequencing-based diversity studies.CrossRef | 1:CAS:528:DC%2BC3sXhsFagtQ%3D%3D&md5=fe48f8393eee7142d647933ea7750ef2CAS |

Kuczynski J, Stombaugh J, Walters WA, González A, Caporaso JG, Knight R (2012) Using QIIME to analyze 16S rRNA gene sequences from microbial communities. In ‘Current Protocols in Microbiology’ Chapter 1, Unit 1E.5. 10.1002/9780471729259.mc01e05s27

Lozupone C, Lladser ME, Knights D, Stombaugh J, Knight R (2011) UniFrac: an effective distance metric for microbial community comparison. The ISME Journal 5, 169–172.
UniFrac: an effective distance metric for microbial community comparison.CrossRef |

Martirosyan V, Unc A, Miller G, Doniger T, Wachtel C, Steinberger Y (2016) Desert perennial shrubs shape the microbial-community miscellany in laimosphere and phyllosphere space. Microbial Ecology 72, 659–668.
Desert perennial shrubs shape the microbial-community miscellany in laimosphere and phyllosphere space.CrossRef |

Noy-Meir I (1973) Desert ecosystems: environment and producers. Annual Review of Ecology and Systematics 4, 25–51.
Desert ecosystems: environment and producers.CrossRef |

Noy-Meir I (1974) Desert ecosystems: higher trophic levels. Annual Review of Ecology and Systematics 5, 195–214.
Desert ecosystems: higher trophic levels.CrossRef |

Olsen SR, Watanabe FS (1957) A Method to Determine a Phosphorus Adsorption Maximum of Soils as Measured by the Langmuir Isotherm1. Soil Science Society of America Journal 21, 144
A Method to Determine a Phosphorus Adsorption Maximum of Soils as Measured by the Langmuir Isotherm1.CrossRef | 1:CAS:528:DyaG2sXntlKltA%3D%3D&md5=f0336d8480425e266b4e46c9f42dc4a2CAS |

Reynolds JF, Virginia RA, Kemp PR, de Soyza AG, Tremmel DC (1999) Impact of drought on desert shrubs: effects of seasonality and degree of resource island development. Ecological Monographs 69, 69–106.
Impact of drought on desert shrubs: effects of seasonality and degree of resource island development.CrossRef |

Robinson BS, Bamforth SS, Dobson PJ (2002) Density and diversity of protozoa in some arid Australian soils. The Journal of Eukaryotic Microbiology 49, 449–453.
Density and diversity of protozoa in some arid Australian soils.CrossRef |

Saul-Tcherkas V, Steinberger Y (2011) Soil microbial diversity in the vicinity of a Negev Desert shrub—Reaumuria negevensis. Microbial Ecology 61, 64–81.
Soil microbial diversity in the vicinity of a Negev Desert shrub—Reaumuria negevensis.CrossRef |

Schlesinger WH, Raikes JA, Hartley AE, Cross AF (1996) On the spatial pattern of soil nutrients in desert ecosystems. Ecology 77, 364
On the spatial pattern of soil nutrients in desert ecosystems.CrossRef |

Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, Sahl JW, Stres B, Thallinger GG, Van Horn DJ, Weber CF (2009) Introducing MOTHER: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Applied and Environmental Microbiology 75, 7537–7541.
Introducing MOTHER: open-source, platform-independent, community-supported software for describing and comparing microbial communities.CrossRef | 1:CAS:528:DC%2BC3cXis1yltw%3D%3D&md5=7843d398f8266dfe5ef2a946e7040215CAS |

Sikorski J, Nevo E (2005) Adaptation and incipient sympatric speciation of Bacillus simplex under microclimatic contrast at ‘Evolution Canyons’ I and II, Israel. Proceedings of the National Academy of Sciences of the United States of America 102, 15924–15929.
Adaptation and incipient sympatric speciation of Bacillus simplex under microclimatic contrast at ‘Evolution Canyons’ I and II, Israel.CrossRef | 1:CAS:528:DC%2BD2MXht1Wru7fI&md5=ef74fa4bcde3709a3ade7c15de6b1b73CAS |

Sternberg M, Shoshany M (2001) Influence of slope aspect on Mediterranean woody formations: Comparison of a semiarid and an arid site in Israel. Ecological Research 16, 335–345.
Influence of slope aspect on Mediterranean woody formations: Comparison of a semiarid and an arid site in Israel.CrossRef |

Steven B, Gallegos-Graves LV, Yeager C, Belnap J, Kuske CR (2014a) Common and distinguishing features of the bacterial and fungal communities in biological soil crusts and shrub root zone soils. Soil Biology & Biochemistry 69, 302–312.
Common and distinguishing features of the bacterial and fungal communities in biological soil crusts and shrub root zone soils.CrossRef | 1:CAS:528:DC%2BC2cXisVCisQ%3D%3D&md5=c210d8383c38be2cc02ab5faf30cb512CAS |

Steven B, Gallegos-Graves LV, Yeager C, Belnap J, Kuske CR (2014b) Common and distinguishing features of the bacterial and fungal communities in biological soil crusts and shrub root zone soils. Soil Biology & Biochemistry 69, 302–312.
Common and distinguishing features of the bacterial and fungal communities in biological soil crusts and shrub root zone soils.CrossRef | 1:CAS:528:DC%2BC2cXisVCisQ%3D%3D&md5=c210d8383c38be2cc02ab5faf30cb512CAS |

Yu J, Steinberger Y (2011) Vertical distribution of microbial community functionality under the canopies of Zygophyllum dumosum and Hammada scoparia in the Negev Desert, Israel. Microbial Ecology 62, 218–227.
Vertical distribution of microbial community functionality under the canopies of Zygophyllum dumosum and Hammada scoparia in the Negev Desert, Israel.CrossRef |



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