Abstract
Agave lechuguilla is a widely distributed plant in arid ecosystems. It has been suggested that its microbiome is partially responsible for its great adaptability to the oligotrophic environments of the Chihuahuan Desert. To lead the recruitment of beneficial rhizobacteria, the root exudates are essential; however, the amino acids contained within these compounds had been largely overlooked. Thus, we investigated how the variations of amino acids in the rhizosphere at different growth stages of A. lechuguilla affect the rhizobacterial community composition, its functions, and activity of the beneficial bacteria. In this regard, it was found that arginine and tyrosine were related to the composition of the rhizobacterial community associated to A. lechuguilla, where the most abundant genera were from the phylum Proteobacteria and Bacteroidetes. Moreover, Firmicutes was largely represented by Bacillus in the phosphorus-mineralizing bacteria community, which may indicate its great distribution and versatility in the harsh environments of the Chihuahuan Desert. In contrast, we found a high proportion of Unknown taxa of nitrogen-fixing bacteria, reflecting the enormous diversity in the rhizosphere of these types of plants that remains to be explored. This work also reports the influence of micronutrients and the amino acids methionine and arginine over the increased activity of the nitrogen-fixing and phosphorus-mineralizing bacteria in the rhizosphere of lechuguillas. In addition, the results highlight the multiple beneficial functions present in the microbiome that could help the host to tolerate arid conditions and improve nutrient availability.
Similar content being viewed by others
Data Availability
The raw sequences obtained from Illumina sequencing of 16S rRNA, nifH, and phoD gene amplicons are available in the GenBank Sequence Read Archive under the Bioproject accession PRJNA672793. R codes are available on request.
References
Houri A, Machaka-Houri N (2016) Agave lechuguilla as a potential biomass source in arid areas. J Sustain Dev Energy Water Environ Syst 4:89–93. https://doi.org/10.13044/j.sdewes.2016.04.0008
Behnke R, Mortimore M (2016) The end of desertification? Springer, Berlin, Heidelberg
Vurukonda S, Vardharajula S, Shrivastava M et al (2016) Enhancement of drought stress tolerance in crops by plant growth promoting rhizobacteria. Microbiol Res 184:13–24. https://doi.org/10.1016/j.micres.2015.12.003
Tao Q, Hou D, Yang X, Li T (2016) Oxalate secretion from the root apex of Sedum alfredii contributes to hyperaccumulation of Cd. Plant Soil 398:139–152. https://doi.org/10.1007/s11104-015-2651-x
Li K, Liu R, Zhang H, Yun J (2013) The diversity and abundance of bacteria and oxygenic phototrophs in saline biological desert crusts in Xinjiang, Northwest China. Microb Ecol 66:40–48. https://doi.org/10.1007/s00248-012-0164-1
Ray S, Mishra S, Bisen K et al (2018) Modulation in phenolic root exudate profile of Abelmoschus esculentus expressing activation of defense pathway. Microbiol Res 207:100–107. https://doi.org/10.1016/j.micres.2017.11.011
Rahmoune B, Zerrouk I, Bouzaa S et al (2019) Amino acids profiling in Datura stramonium and study of their variations after inoculation with plant growth promoting rhizobacteria. Biologia 74:1373–1383. https://doi.org/10.2478/s11756-019-00287-y
Ma H, Pei G, Gao R et al (2017) Mineralization of amino acids and its signs in nitrogen cycling of forest soil. Acta Ecol Sin 37:60–63. https://doi.org/10.1016/j.chnaes.2016.09.001
Rabe E, Lovatt C (1986) Increased arginine biosynthesis during phosphorus deficiency. Plant physiol 81:774–779. https://doi.org/10.1104/pp.81.3.774
Yoneyama T, Terakado-Tonooka J, Minamisawa K (2017) Exploration of bacterial N2-fixation systems in association with soil-grown sugarcane, sweet potato, and paddy rice: a review and synthesis. Soil Sci Plan Nutr 63:578–590. https://doi.org/10.1080/00380768.2017.1407625
Hennion N, Durand M, Vriet C et al (2019) Sugars en route to the roots. Transport, metabolism and storage within plant roots and towards microorganisms of the rhizosphere. Physiol Plant 165:44–57. https://doi.org/10.1111/ppl.12751
Badri DV, Vivanco JM (2009) Regulation and function of root exudates. Plant Cell Environ 32:666–681. https://doi.org/10.1111/j.1365-3040.2009.01926.x
Hildebrandt TM, Nunes Nesi A, Araújo WL et al (2015) Amino acid catabolism in plants. Mol Plant 8:1563–1579. https://doi.org/10.1016/j.molp.2015.09.005
Carvalhais LC, Dennis PG, Badri DV et al (2013) Activation of the jasmonic acid plant defense pathway alters the composition of rhizosphere bacterial communities. PLoS ONE 8:1–5. https://doi.org/10.1371/journal.pone.0056457
Yuan J, Zhao J, Wen T et al (2018) Root exudates drive the soil-borne legacy of aboveground pathogen infection. Microbiome 6:1–12. https://doi.org/10.1186/s40168-018-0537-x
Barret M, Morrissey JP, O’Gara F (2011) Functional genomics analysis of plant growth-promoting rhizobacterial traits involved in rhizosphere competence. Biol Fertil Soils 47:729–743. https://doi.org/10.1007/s00374-011-0605-x
Hutapea PS, Abdullah L, Karti PDMH et al (2018) Improvement of Indigofera zollingeriana production and methionine content through inoculation of nitrogen-fixing bacteria. Trop Anim Sci J 41:37–45. https://doi.org/10.5398/TASJ.2018.41.1.37
Miltner A, Kindler R, Knicker H et al (2009) Fate of microbial biomass-derived amino acids in soil and their contribution to soil organic matter. Org Geochem 40:978–985. https://doi.org/10.1016/j.orggeochem.2009.06.008
Huo C, Luo Y, Cheng W (2017) Rhizosphere priming effect: a meta-analysis. Soil Biol Biochem 111:78–84. https://doi.org/10.1016/j.soilbio.2017.04.003
Jones DL, Darrah PR (1994) Amino-acid influx at the soil-root interface of Zea mays L. and its implications in the rhizosphere. Plant Soil 163:1–12. https://doi.org/10.1007/BF00033935
Moe LA (2013) Amino acids in the rhizosphere: from plants to microbes. Am J Bot 100:1692–1705. https://doi.org/10.3732/ajb.1300033
Oku S, Komatsu A, Tajima T et al (2012) Identification of chemotaxis sensory proteins for amino acids in Pseudomonas fluorescens Pf0-1 and their involvement in chemotaxis to tomato root exudate and root colonization. Microbes Environ 27:462–469. https://doi.org/10.1264/jsme2.ME12005
Ayangbenro AS, Babalola OO (2021) Reclamation of arid and semi-arid soils: the role of plant growth-promoting archaea and bacteria. Curr Plant Biol 25:100173. https://doi.org/10.1016/j.cpb.2020.100173
López-Lozano NE, Echeverría-Molinar A, Ortiz-Durán EA et al (2020) Bacterial diversity and interaction networks of Agave lechuguilla rhizosphere differ significantly from bulk soil in the oligotrophic Basin of Cuatro Ciénegas. Front Plant Sci 11:1028. https://doi.org/10.3389/fpls.2020.01028
Medina-de la Rosa G, García-Oliva F, Alpuche-Solís ÁG et al (2021) The nutrient-improvement bacteria selected by Agave lechuguilla T. and their role in the rhizosphere community. FEMS Microbiol 97:1–14. https://doi.org/10.1093/femsec/fiab137
Zheng L, Dean DR (1994) Catalytic formation of a nitrogenase iron-sulfur cluster. J Biol Chem 269:18723–18726. https://doi.org/10.1016/s0021-9258(17)32225-1
Zehr JP, Turner PJ (2001) Nitrogen fixation: nitrogenase genes and gene expression. Methods Microbiol 30:271–286. https://doi.org/10.1016/S0580-9517(01)30049-1
Zehr JP, Jenkins BD, Short SM et al (2003) Nitrogenase gene diversity and microbial community structure: a cross-system comparison. Environ Microbiol 5:539–554. https://doi.org/10.1046/j.1462-2920.2003.00451.x
Abu-Zaitoon Y, Abdul-Karim S (2012) Ecological studies on nitrogen fixing bacteria from leguminous plants at the north of Jordan. Afr J Microbiol Res 6:3656–3661. https://doi.org/10.5897/AJMR12.098
González-López J, Rodelas B, Pozo C et al (2005) Liberation of amino acids by heterotrophic nitrogen fixing bacteria. Amino Acids 28:363–367. https://doi.org/10.1007/s00726-005-0178-9
Perroni Y, García-Oliva F, Tapia-Torres Y et al (2014) Relationship between soil P fractions and microbial biomass in an oligotrophic grassland-desert scrub system. Ecol Res 29:463–472. https://doi.org/10.1007/s11284-014-1138-1
García-Oliva F, Merino A, Fonturbel MT et al (2018) Severe wildfire hinders renewal of soil P pools by thermal mineralization of organic P in forest soil: analysis by sequential extraction and 31P NMR spectroscopy. Geoderma 309:32–40. https://doi.org/10.1016/j.geoderma.2017.09.002
Chen X, Jiang N, Chen Z et al (2017) Response of soil phoD phosphatase gene to long-term combined applications of chemical fertilizers and organic materials. Appl Soil Ecol 119:197–204. https://doi.org/10.1016/j.apsoil.2017.06.019
Carvalhais LC, Dennis PG, Fan B et al (2013) Linking plant nutritional status to plant-microbe interactions. PLoS ONE 8:1–13. https://doi.org/10.1371/journal.pone.0068555
Trame A-M, Coddington AJ, Paige KN (1995) Field and genetic studies testing optimal outcrossing in Agave schottii, a long-lived clonal plant. Oecologia 104:93–100. https://doi.org/10.1007/BF00365567
SEMARNAT (2002) Norma Oficial Mexicana Nom-021-Semarnat-2000 Que establece las especificaciones de fertilidad, salinidad y clasificación de suelos, estudio, muestreo y análisis. Diario Oficial de la Federación. http://faolex.fao.org/docs/pdf/mex50674.pdf. Accessed 08 Octuber 2022
Schubert CJ, Nielsen B (2000) Effects of decarbonation treatments on δ13C values in marine sediments. Mar Chem 72:55–59. https://doi.org/10.1016/S0304-4203(00)00066-9
Bray RH, Kurtz LT (1945) Determination of total, organic, and available forms of phosphorus in soils. Soil Sci 59:39–46. https://doi.org/10.1097/00010694-194501000-00006
Nelson DW (1983) Determination of ammonium in KCl extracts of soils by the salicylate method. Commun Soil Sci Plant Anal 14:1051–1062. https://doi.org/10.1080/00103628309367431
García-Robledo E, Corzo A, Papaspyrou S (2014) A fast and direct spectrophotometric method for the sequential determination of nitrate and nitrite at low concentrations in small volumes. Mar Chem 162:30–36. https://doi.org/10.1016/j.marchem.2014.03.002
Lindsay WL, Norvell WA (1978) Development of a DTPA soil test for zinc, iron, manganese, and copper. SSSAJ 42:421–428. https://doi.org/10.2136/sssaj1978.03615995004200030009x
Turner S, Pryer KM, Miao VPW et al (1999) Investigating deep phylogenetic relationships among Cyanobacteria and plastids by small subunit rRNA sequence analysis. J Eukaryot Microbiol 46:327–338. https://doi.org/10.1111/j.1550-7408.1999.tb04612.x
Rudi K, Skulberg OM, Larsen F et al (1997) Strain characterization and classification of oxyphotobacteria in clone cultures on the basis of 16S rRNA sequences from the variable regions V6, V7, and V8. Appl Environ Microbiol 63:2593–2599. https://doi.org/10.1128/AEM.63.7.2593-2599.1997
R Core Team (2020) R: A language and environment for statistical computing
Wemheuer F, Taylor JA, Daniel R et al (2020) Tax4Fun2: prediction of habitat-specific functional profiles and functional redundancy based on 16S rRNA gene sequences. Environ Microbiome 15:11. https://doi.org/10.1186/s40793-020-00358-7
López-Lozano NE, Carcaño-Montiel MG, Bashan Y (2016) Using native trees and cacti to improve soil potential nitrogen fixation during long-term restoration of arid lands. Plant Soil 403:317–329. https://doi.org/10.1007/s11104-016-2807-3
Eivazi F, Tabatabai MA (1977) Phosphatases in soil. Soil Biol Biochem 9:167–172. https://doi.org/10.1016/0038-0717(77)90070-0
Poly F, Monrozier LJ, Bally R (2001) Improvement in the RFLP procedure for studying the diversity of nifH genes in communities of nitrogen fixers in soil. Res Microbiol 152:95–103. https://doi.org/10.1016/S0923-2508(00)01172-4
Simonet P, Grosjean MC, Misra AK et al (1991) Frankia genus-specific characterization by polymerase chain reaction. Appl Environ Microbiol 57:3278–3286. https://doi.org/10.1128/AEM.57.11.3278-3286.1991
Ragot SA, Kertesz MA, Bünemann EK (2015) phoD alkaline phosphatase gene diversity in soil. Appl Environ Microbiol 81:7281–7289. https://doi.org/10.1128/AEM.01823-15
Oksanen J, Blanchet FG, Friendly M et al (2020) vegan: Community ecology package
Mapelli F, Marasco R, Fusi M et al (2018) The stage of soil development modulates rhizosphere effect along a High Arctic desert chronosequence. ISME J 12:1188–1198. https://doi.org/10.1038/s41396-017-0026-4
Granados-Sánchez D, Sánchez-González A, Granados-Victorino RL et al (2011) Ecología de la vegetación del Desierto Chihuahuense. Rev Chapingo Ser Cienc For Ambiente 17:111–130. https://doi.org/10.5154/r.rchscfa.2010.10.102
Bashan Y, De-Bashan LE (2010) Microbial populations of arid lands and their potential for restoration of deserts. In: Dion P (ed) Soil biology and agriculture in the tropic. Springer, Berlin, pp 109–137
Liu W, Ling N, Guo J et al (2020) Legacy effects of 8-year nitrogen inputs on bacterial assemblage in wheat rhizosphere. Biol Fertil Soils 56:583–596. https://doi.org/10.1007/s00374-020-01435-2
Bull AT, Asenjo JA, Goodfellow M et al (2016) The Atacama Desert: technical resources and the growing importance of novel microbial diversity. Annu Rev Microbiol 70:215–234. https://doi.org/10.1146/annurev-micro-102215-095236
Othmany RE, Zahir H, Ellouali M et al (2021) Current understanding on adhesion and biofilm development in Actinobacteria. Int J Micrbiol 2021:1–11. https://doi.org/10.1155/2021/6637438
Rateb ME, Ebel R, Jaspars M (2018) Natural product diversity of actinobacteria in the Atacama Desert. Antonie Van Leeuwenhoek 111:1467–1477. https://doi.org/10.1007/s10482-018-1030-z
Kindaichi T, Yuri S, Ozaki N et al (2012) Ecophysiological role and function of uncultured Chloroflexi in an anammox reactor. Water Sci Technol 66:2556–2561. https://doi.org/10.2166/wst.2012.479
Witte CP (2011) Urea metabolism in plants. Plant Sci 180:431–438. https://doi.org/10.1016/j.plantsci.2010.11.010
Ninomiya A, Murata Y, Tada M et al (2004) Changes in allantoin and arginine contents in Dioscorea opposita “Tsukuneimo” during the growth. Engei Gakkai zasshi 73:546–551. https://doi.org/10.2503/jjshs.73.546
Feng H, Zhang N, Du W et al (2018) Identification of chemotaxis compounds in root exudates and their sensing chemoreceptors in plant-growth-promoting rhizobacteria Bacillus amyloliquefaciens SQR9. Mol Plant Microbe Interact 31:995–1005. https://doi.org/10.1094/MPMI-01-18-0003-R
Schenck CA, Maeda HA (2018) Tyrosine biosynthesis, metabolism, and catabolism in plants. Phytochemistry 149:82–102
Obata T, Fernie AR (2012) The use of metabolomics to dissect plant responses to abiotic stresses. Cell Mol Life Sci 69:3225–3243. https://doi.org/10.1007/s00018-012-1091-5
Rengel Z (2015) Availability of Mn, Zn and Fe in the rhizosphere. J Soil Sci Plant Nutr 15:397–409. https://doi.org/10.4067/S0718-95162015005000036
Kamran S, Shahid I, Baig DN et al (2017) Contribution of zinc solubilizing bacteria in growth promotion and zinc content of wheat. Front Microbiol 8:2593. https://doi.org/10.3389/fmicb.2017.02593
Eshaghi E, Nosrati R, Owlia P et al (2019) Zinc solubilization characteristics of efficient siderophore-producing soil bacteria. Iran J Microbiol 11:419–430. https://doi.org/10.18502/ijm.v11i5.1961
Saravanakumar D, Samiyappan R (2007) ACC deaminase from Pseudomonas fluorescens mediated saline resistance in groundnut (Arachis hypogea) plants. J Appl Microbiol 102:1283–1292. https://doi.org/10.1111/j.1365-2672.2006.03179.x
Meena VS (2018) Role of rhizospheric microbes in soil. Springer Singapore
Gaby JC, Buckley DH (2014) A comprehensive aligned nifH gene database: a multipurpose tool for studies of nitrogen-fixing bacteria. Database 2014:1–8. https://doi.org/10.1093/database/bau001
Coskun D, Britto DT, Shi W et al (2017) How plant root exudates shape the nitrogen cycle. Trends Plant Sci 22:661–673. https://doi.org/10.1016/j.tplants.2017.05.004
Herrero A, Muro-Pastor AM, Flores E (2001) Nitrogen control in Cyanobacteria. J Bacteriol 183:411–425. https://doi.org/10.1128/JB.183.2.411-425.2001
Mandon K, Østerås M, Boncompagni E et al (2003) The Sinorhizobium meliloti glycine betaine biosynthetic genes (betICBA) are induced by choline and highly expressed in bacteroids. Mol Plant Microbe Interact 16:709–719. https://doi.org/10.1094/MPMI.2003.16.8.709
Spaepen S, Dobbelaere S, Croonenborghs A et al (2008) Effects of Azospirillum brasilense indole-3-acetic acid production on inoculated wheat plants. Plant Soil 312:15–23. https://doi.org/10.1007/s11104-008-9560-1
Bahuguna RN, Pal M (2011) Physiology of nitrogen fixation in legumes under elevated CO2. In: Singh MP, Khetarpal S, Pandey R et al (eds) Climate change: impacts and adaptations in crop plants. Today and tomorrow, New Delhi, pp 213–228
Byer AS, Shepard EM, Peters JW et al (2015) Radical S-adenosyl-l-methionine chemistry in the synthesis of hydrogenase and nitrogenase metal cofactors. J Biol Chem 290:3987–3994. https://doi.org/10.1074/jbc.R114.578161
Phillips DA, Fox TC, King MD et al (2004) Microbial products trigger amino acid exudation from plant roots. Plant Physiol 136:2887–2894. https://doi.org/10.1104/pp.104.044222
Rodríguez MD, Alcaraz LD, Souza V et al (2018) Single genus approach to understanding bacterial diversity, niche, distribution, and genomics: the Bacillus in Cuatro Ciénegas. In: Souza V, Eguiarte LE, Olmedo-Álvarez G (eds) Cuatro Ciénegas Ecology, natural history and microbiology. Springer, Switzerland, pp 103–112
Tapia-Torres Y, Rodríguez-Torres MD, Elser JJ et al (2016) How to live with phosphorus scarcity in soil and sediment: lessons from bacteria. Appl Environ Microbiol 82:4652–4662. https://doi.org/10.1128/AEM.00160-16
Tapia-Torres Y, Olmedo-Álvarez G (2018) Life on phosphite: a metagenomics tale. Trends Microbiol 26:170–172. https://doi.org/10.1016/j.tim.2018.01.002
Zappa S, Rolland JL, Flament D et al (2001) Characterization of a highly thermostable alkaline phosphatase from the Euryarchaeon Pyrococcus abyssi. Appl Environ Microbiol 67:4504–4511. https://doi.org/10.1128/AEM.67.10.4504-4511.2001
Su J-Q, Ding L-J, Xue K et al (2015) Long-term balanced fertilization increases the soil microbial functional diversity in a phosphorus-limited paddy soil. Mol Ecol 24:136–150. https://doi.org/10.1111/mec.13010
Morris SM (2004) Enzymes of arginine metabolism. J Nutr 134:2743S-2747S. https://doi.org/10.1093/jn/134.10.2743S
Si Z, Guan N, Zhou Y et al (2020) A methionine sulfoxide reductase B is required for the establishment of Astragalus sinicus–Mesorhizobium symbiosis. Plant Cell Physiol 61:1631–1645. https://doi.org/10.1093/pcp/pcaa085
Spohn M, Ermak A, Kuzyakov Y (2013) Microbial gross organic phosphorus mineralization can be stimulated by root exudates – a 33P isotopic dilution study. Soil Biol Biochem 65:254–263. https://doi.org/10.1016/j.soilbio.2013.05.028
Tavakoli R, Rastegar S, Khaledi M et al (2019) Investigating effect of amino acids leucine, valine and alanine on alkaline phosphatase activity of purified acetone fractions of sweet lemon, garlic and onion. Int J Ayurvedic Med 10:34–38
Bodansky O (1948) The inhibitory effects of DL-alanine, L-glutamic acid, L-lysine, and L-histidine on the activity of intestinal, bone and kidney phosphatases. J Biol Chem 174:465–476. https://doi.org/10.1016/S0021-9258(18)57328-2
So PPL, Tsui FWL, Vieth R et al (2007) Implications for calcium pyrophosphate dihydrate crystal deposition disease. J Rheumatol 34:1313–1322
Acknowledgements
GMR thanks CONACyT for the Ph.D. scholarship grant 332648. We want to thank Juan Pablo Rodas Ortíz, Guillermo Vidriales Escobar, and Ma. del Carmen Rocha Medina for technical support during the development of this project.
Funding
The authors acknowledge the funding of SEP-CONACyT Basic Science 254406 to NELL.
Author information
Authors and Affiliations
Contributions
NELL contributed to the study conception and design. GMDR, NELL, and FGO performed the data collection, general analysis, interpretation, and draft of the paper. FGO coordinated the enzymatic activities and physicochemical soil properties analysis. COV coordinated the sequence analysis and functional predictions. LBC and LLR contributed to the identification of the amino acids in root exudates and performed data interpretation. All authors reviewed the article and approved the submitted version.
Corresponding author
Ethics declarations
Conflict of Interest
The authors declare no competing interests.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
la Rosa, G.Md., García-Oliva, F., Ovando-Vázquez, C. et al. Amino Acids in the Root Exudates of Agave lechuguilla Torr. Favor the Recruitment and Enzymatic Activity of Nutrient-Improvement Rhizobacteria. Microb Ecol 86, 1176–1188 (2023). https://doi.org/10.1007/s00248-022-02162-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00248-022-02162-x