Abstract
Arica and Parinacota Region is located at the extreme north of the Atacama Desert, where the high levels of salts and boron, lack of rain, high UV radiation, among other conditions, make this zone an extreme environment. Despite these characteristics, in the transversal valleys, different types of crops are cultivated in this region, which are associated to beneficial microorganisms with specific traits that allow plants surviving and developing under extreme conditions. However, there is incomplete information related to these microorganisms. In this work, bacteria associated with ancestral crops were isolated from oregano, alfalfa, maize, potato, and grapevine samples from Belén, Codpa, Molinos, Poconchile and Socoroma localities, representing the first report of these microorganisms in those sites. Bacteria were identified, being γ-Proteobacteria, the most frequent class (~ 74.4%), with members of Pseudomonas genus the most common isolated genus. All bacteria were functionally characterized for plant growth-promoting activities, including siderophores and auxins production, phosphate solubilization, and nitrogen fixation, revealing an extraordinary potential from these microorganisms for agricultural applications under arid and semiarid conditions.
Similar content being viewed by others
Abbreviations
- ACC:
-
1-Aminocyclopropane-1-carboxylate
- EC:
-
Electrical conductivity
- CAS:
-
Chrome Azurol S
- IAA:
-
Indole-3-acetic acid
- PVK:
-
Pikovskaya solid medium
References
Acuña-Rodríguez I, Hansen H, Gallardo-Cerda J, Atala C, Molina-Montenegro M (2019) Antarctic extremophiles: biotechnological alternative to crop productivity in saline soils. Front Bioeng Biotech 7:22
Altschul S, Gish W, Miller W, Myers E, Lipman D (1990) Basic local alignment search tool. J Mol Biol 215:403–410
Berg G, Grube M, Schloter M, Smalla K (2014) Unraveling the plant microbiome: looking back and future perspectives. Front Microbiol 5:148
Bull A, Andrews B, Dorador C, Goodfellow M (2018) Introducing the Atacama Desert. Antonie Van Leeuwenhoek 111(8):1269–1272
Castro J, Razmilic V, Gomez-Escribano J, Andrews B, Asenjo J, Bibb M (2018) The ‘gifted’ actinomycete Streptomyces leeuwenhoekii. Antonie Van Leeuwenhoek 111(8):1433–1448
Caulier S, Nannan C, Gillis A, Licciardi F, Bragard C, Mahillon J (2019) Overview of the antimicrobial compounds produced by members of the Bacillus subtilis group. Front Microbiol 10:302
Cornejo L (2009) Recursos hídricos y desarrollo socioeconómico en zonas áridas: importancia y perspectivas de nuevas tecnologías aplicadas al tratamiento de aguas naturales y/o residuales. Ingeniare Revista Chilena de Ingeniería 17(3):285–287
Dorador C, Fink P, Hengst M, Icaza G, Villalobos A, Vejar D et al (2018) Microbial community composition and trophic role along a marked salinity gradient in Laguna Puilar, Salar de Atacama. Chile Antonie van Leeuwenhoek 111(8):1361–1374
Dutkiewicz J, Mackiewicz B, Lemieszek M, Golec M, Milanowski J (2016) Pantoea agglomerans: a mysterious bacterium of evil and good. Part IV. Beneficial effects. Ann Agric Environ Med. 23(2):206–222
Ehmann A (1977) The Van Urk-Salkowski reagent-a sensitive and specific chromogenic reagent for silica gel thin-layer chromatographic detection and identification of indole derivatives. J Chromatog 132:267–276
El Amrani A, Dumas A, Wick L, Yergeau E, Berthomé R (2015) “Omics” insights into PAH degradation toward improved green remediation biotechnologies. Environ Sci Technol 49:1128–11291
Fernández-Martínez M, dos Santos SR, Moreno-Paz M, Gallardo-Carreño I, Blanco Y, Warren-Rhodes K, García-Villadangos M, Ruiz-Bermejo M, Barberán A, Wettergreen D, Cabrol N, Parro V (2019) Prokaryotic community structure and metabolisms in shallow subsurface of Atacama Desert playas and alluvial fans after heavy rains: repairing and preparing for next dry period. Front Microbiol 10:1641
Frank J, Reich C, Sharma S, Weisbaum J, Wilson B, Olsen G (2008) Critical evaluation of two primers commonly used for amplification of bacterial 16S rRNA genes. Appl Environ Microbiol 74:2461–2470
Fuentes A, Herrera H, Charles T, Arriagada C (2020) Fungal and bacterial microbiome associated with the rhizosphere of native plants from the Atacama Desert. Microorganisms 8:209
Gadhave K, Gange A (2016) Plant-associated Bacillus spp. alter life-history traits of the specialist insect Brevicoryne brassicae L. Agric For Entomol 18(1):35–42
Gómez-Silva B (2018) Lithobiontic life: “Atacama rocks are well and alive.” Antonie Van Leeuwenhoek 111(8):1333–1343
Goodfellow M, Nouioui I, Sanderson R, Xie F, Bull A (2018) Rare taxa and dark microbial matter: novel bioactive actinobacteria abound in Atacama Desert soils. Antonie Van Leeuwenhoek 111(8):1315–1332
Han Y, Wang R, Yang Z, Zhan Y, Ma Y, Ping S, Zhang L, Lins M, Yin Y (2015) 1-aminocyclopropane-1-carboxylate deaminase from Pseudomonas stutzeri A1501 facilitates the growth of rice in the presence of salt or heavy metals. J Microbiol Biotechnol 25(7):1119–1128
Kalayu G (2019) Phosphate solubilizing microorganisms: promising approach as biofertilizers. Int J Agr 2019:4917256
King E, Ward M, Raney D (1954) Two simple media for the demonstration of pyocyanin and fluorescin. J Lab Clin Med 44:301–307
Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33(7):1870–1874
Larkin M, Blackshields G, Brown N, Chenna R, McGettigan P, McWilliam H et al (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23:2947–2948
Malik D, Sindhu S (2011) Production of indole acetic acid by Pseudomonas sp.: effect of coinoculation with Mesorhizobium sp. Cicer on nodulation and plant growth of chickpea (Cicer arietinum). Physiol Mol Biol Plants 17(1):25–32
Maza F, Maldonado J, Vásquez-Dean J, Mandakovic D, Gaete A, Cambiazo V, González M (2019) Soil bacterial communities from the Chilean Andean highlands: taxonomic composition and culturability. Front Bioeng Biotechnol 7:10
Meteochile (2020) Informe climatológico nacional. Meteochile Website https://climatologia.meteochile.gob.cl/application/diario/boletinClimatologicoDiario/actual
Muggia L, Zalar P, Azua-Bustos A, González-Silva C, Grube M, Gunde-Cimerman N (2020) The beauty and the yeast: can the microalgae Dunaliella form a borderline lichen with Hortaea werneckii? Symbiosis. https://doi.org/10.1007/s13199-020-00697-6
Muñoz P, Márquez S, González-Nilo F, Márquez-Miranda V, Blamey J (2017) Structure and application of antifreeze protein from Antarctic bacteria. Microb Cell Fact 16:138
Neupane S, Finlay R, Kyrpides N, Goodwin L, Alström S et al (2012) Complete genome sequence of the plant-associated Serratia plymuthica strain AS13. Stand Genomic Sci 7(1):22–30
ODEPA (2018) Región de Arica y Parinacota: información regional 2018. ODEPA Website https://www.odepa.gob.cl/wp-content/uploads/2018/02/Arica-y-Parinacota.pdf
Orellana R, Macaya C, Bravo G, Dorochesi F, Cumsille A, Valencia R et al (2018) Living at the frontiers of life: extremophiles in Chile and their potential for bioremediation. Front Microbiol 9:2309
Pikovskaya R (1948) Mobilization of phosphorus in soil in connection with the vital activity of some microbial species. Microbiology 17:362–370
Qessaoui R, Bouharroud R, Furze J, El Aalaoui M, Akroud H, Amarraque A, Van Vaerenbergh J, Tahzima R, Mayad E, Chebli B (2019) Applications of new rhizobacteria Pseudomonas isolates in agroecology via fundamental processes complementing plant growth. Sci Rep 9:12832
Qin Y, Druzhinina I, Pan X, Yuan Z (2016) Microbially mediated plant salt tolerance and microbiome-based solutions for saline agriculture. Biotech Adv 34:1245–1259
Radhakrishnan R, Hashem A, Abd_allh E (2017) Bacillus: a biological tool for crop improvement through bio-molecular changes in adverse environments. Front Physiol 8:667
Rateb M, Ebel R, Jaspars M (2018) Natural product diversity of actinobacteria in the Atacama Desert. Antonie Van Leeuwenhoek 111(8):1467–1477
Rodríguez E (1982) Improved medium for isolation of Azospirillum spp. Appl Environ Microbiol 44(4):990–991
Ruginescu R, Purcārea C, Dorador C, Lavin P, Cojoc R, Neagu S, Lucaci I, Enache M (2019) Exploring the hydrolytic potential of cultured halophilic bacteria isolated from the Atacama Desert. FEMS Microbiol Let 366(17):fnz224
Sadzawka A, Carrasco M, Grez R, De la luz M, Flores H, Neaman A (2006) Métodos de análisis recomendados para los suelos de Chile. Instituto de Investigaciones Agropecuarias, Series Actas INIA 34. https://biblioteca.inia.cl/link.cgi/Catalogo/Actas/448.act
Salvatierra-Martínez R, Sepúlveda-Chavera G, Huanca-Mamani W, Rodríguez-Molina M (2015) Native strains of Trichoderma from northern Chile: adaptive tolerance in boric saline soils. Interciencia 40(4):263–269
Santiago I, Gonçalves V, Gómez-Silva B, Galetovic A, Rosa L (2018) Fungal diversity in the Atacama Desert. Antonie Van Leeuwenhoek 111(8):1345–1360
Sasirekha B, Srividya S (2016) Siderophore production by Pseudomonas aeruginosa FP6, a biocontrol strain for Rhizoctonia solani and Colletotrichum gloeosporioides causing diseases in chilli. Agric Nat Resour 50(4):250–256
Schwynand B, Neilands J (1987) Universal chemical assay for the detection and determination of siderophores. Anal Biochem 160:47–56
Sepúlveda G, Arismendi-Macuer M, Cárdenas-Ninasivincha S, Huanca-Mamani W, Latorre B (2020) Ocurrence of onion smut caused by Urocystis magica in Chile. Plant Dis. https://doi.org/10.1094/PDIS-04-20-0847-PDN
Tiwari G, Duraivadivel P, Sharma S, Hariprasad P (2018) 1-Aminocyclopropane-1-carboxylic acid deaminase producing beneficial rhizobacteria ameliorate the biomass characters of Panicum maximum Jacq. by mitigating drought and salt stress. Sci Rep 8:17513
Wagi S, Ahmed A (2019) Bacillus spp.: potent microfactories of bacterial IAA. Peer J 7:7258
Wolf A, Fritze A, Hagemann M, Berg G (2002) Stenotrophomonas rhizophila sp. nov., a novel plant-associated bacterium with antifungal properties. Int J Syst Evol Micr 52:1937–1944
Yadav A (2017) Beneficial role of extremophilic microbes for plant health and soil fertility. J Agric Sci Bot 1(1):30–31
Yan X, Wang Z, Mei Y, Wang L, Wang X, Xu Q, Peng S, Zhou Y, Wei C (2018) Isolation, diversity, and growth-promoting activities of endophytic bacteria from tea cultivars of Zijuan and Yunkang-10. Front Microbiol 9:1848
Acknowledgements
This work was supported by the FIC-CORFO Project 13CEI2-21852; and the execution of the Project Co-execution Agreement between the University of Tarapacá and the University of California Davis Chile (“Decreto Exento” N°00.451/2018). Additionally, this manuscript was edited by Mr. Ricardo Reyes Reyes from Editing Office of University of Tarapacá.
Author information
Authors and Affiliations
Contributions
All authors contributed to the study conception and design. Material preparation, sampling, and experimental procedures were performed by PM, MA, SC, DC, FV, and GS. Data analysis were executed by PM and GS. The first draft of the manuscript was written by PM and GS, and all authors commented on previous versions of the manuscript. All authors read and approved the current version of the manuscript.
Corresponding authors
Ethics declarations
Conflict of interest
The authors declare that there are no conflicts of interest.
Human and animal rights
Research involving human participants and animals. The authors declare that this work does not contain any studies performed with humans or animals.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
10482_2020_1482_MOESM1_ESM.xlsx
Online Resource 1 Affiliation of 16S rRNA gene from isolated bacteria associated to crops from Arica and Parinacota Region, Chile. Non submitted sequences to GenBank are indicate as N.S. (XLSX 22 kb)
10482_2020_1482_MOESM2_ESM.pdf
Online Resource 2 Neighbour-joining tree of the partial 16S rRNA gene sequences of the isolated bacteria and their closely related species obtained from GenBank. (PDF 1149 kb)
Rights and permissions
About this article
Cite this article
Muñoz, P.A., Arismendi, M.J., Cárdenas, S.F. et al. Diversity of culturable bacteria isolated from ancestral crops of Arica and Parinacota Region, Atacama Desert. Antonie van Leeuwenhoek 113, 2123–2137 (2020). https://doi.org/10.1007/s10482-020-01482-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10482-020-01482-7