Niche-adaptation in plant-associated Bacteroidetes favours specialisation in organic phosphorus mineralisation.
Journal
The ISME journal
ISSN: 1751-7370
Titre abrégé: ISME J
Pays: England
ID NLM: 101301086
Informations de publication
Date de publication:
04 2021
04 2021
Historique:
received:
24
07
2020
accepted:
30
10
2020
pubmed:
2
12
2020
medline:
22
4
2021
entrez:
1
12
2020
Statut:
ppublish
Résumé
Bacteroidetes are abundant pathogen-suppressing members of the plant microbiome that contribute prominently to rhizosphere phosphorus mobilisation, a frequent growth-limiting nutrient in this niche. However, the genetic traits underpinning their success in this niche remain largely unknown, particularly regarding their phosphorus acquisition strategies. By combining cultivation, multi-layered omics and biochemical analyses we first discovered that all plant-associated Bacteroidetes express constitutive phosphatase activity, linked to the ubiquitous possession of a unique phosphatase, PafA. For the first time, we also reveal a subset of Bacteroidetes outer membrane SusCD-like complexes, typically associated with carbon acquisition, and several TonB-dependent transporters, are induced during Pi-depletion. Furthermore, in response to phosphate depletion, the plant-associated Flavobacterium used in this study expressed many previously characterised and novel proteins targeting organic phosphorus. Collectively, these enzymes exhibited superior phosphatase activity compared to plant-associated Pseudomonas spp. Importantly, several of the novel low-Pi-inducible phosphatases and transporters, belong to the Bacteroidetes auxiliary genome and are an adaptive genomic signature of plant-associated strains. In conclusion, niche adaptation to the plant microbiome thus appears to have resulted in the acquisition of unique phosphorus scavenging loci in Bacteroidetes, enhancing their phosphorus acquisition capabilities. These traits may enable their success in the rhizosphere and also present exciting avenues to develop sustainable agriculture.
Identifiants
pubmed: 33257812
doi: 10.1038/s41396-020-00829-2
pii: 10.1038/s41396-020-00829-2
pmc: PMC8115612
doi:
Substances chimiques
Phosphorus
27YLU75U4W
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
1040-1055Subventions
Organisme : Biotechnology and Biological Sciences Research Council
ID : BB/L026074/1
Pays : United Kingdom
Organisme : Biotechnology and Biological Sciences Research Council
ID : BB/T009152/1
Pays : United Kingdom
Références
Bulgarelli D, Rott M, Schlaeppi K, Ver Loren van Themaat E, Ahmadinejad N, Assenza F, et al. Revealing structure and assembly cues for Arabidopsis root-inhabiting bacterial microbiota. Nature. 2012;488:91–5.
pubmed: 22859207
doi: 10.1038/nature11336
Bulgarelli D, Garrido-Oter R, Münch Philipp C, Weiman A, Dröge J, Pan Y, et al. Structure and function of the bacterial root microbiota in wild and domesticated barley. Cell Host Microbe. 2015;17:392–403.
pubmed: 25732064
pmcid: 4362959
doi: 10.1016/j.chom.2015.01.011
Niu B, Paulson JN, Zheng X, Kolter R. Simplified and representative bacterial community of maize roots. PNAS. 2017;114:e2450–9.
pubmed: 28275097
pmcid: 5373366
doi: 10.1073/pnas.1616148114
Teeling H, Fuchs BM, Becher D, Klockow C, Gardebrecht A, Bennke CM, et al. Substrate-controlled succession of marine bacterioplankton populations induced by a phytoplankton bloom. Science. 2012;336:608–11.
pubmed: 22556258
doi: 10.1126/science.1218344
Thomas F, Hehemann J-H, Rebuffet E, Czjzek M, Michel G. Environmental and gut Bacteroidetes: the food connection. Front Microbiol. 2011;2:93.
pubmed: 21747801
pmcid: 3129010
doi: 10.3389/fmicb.2011.00093
Yin C, Hulbert SH, Schroeder KL, Mavrodi O, Mavrodi D, Dhingra A, et al. Role of bacterial communities in the natural suppression of Rhizoctonia solani bare patch disease of wheat (Triticum aestivum L.). Appl Environ Microbiol. 2013;79:7428–38.
pubmed: 24056471
pmcid: 3837727
doi: 10.1128/AEM.01610-13
Gardner T, Acosta-Martinez V, Senwo Z, Dowd SE. Soil rhizosphere microbial communities and enzyme activities under organic farming in Alabama. Diversity. 2011;3:308–28.
doi: 10.3390/d3030308
Kolton M, Erlacher A, Berg G, Cytryn E. The Flavobacterium genus in the plant holobiont: ecological, physiological, and applicative insights. In: Castro-Sowinski S, editor. Microbial models: from environmental to industrial sustainability. Singapore: Springer Singapore; 2016. p. 189–207.
Maimaiti J, Zhang Y, Yang J, Cen Y-P, Layzell DB, Peoples M, et al. Isolation and characterization of hydrogen-oxidizing bacteria induced following exposure of soil to hydrogen gas and their impact on plant growth. Environ Microbiol. 2007;9:435–44.
pubmed: 17222141
doi: 10.1111/j.1462-2920.2006.01155.x
Kwak M-J, Kong HG, Choi K, Kwon S-K, Song JY, Lee J, et al. Rhizosphere microbiome structure alters to enable wilt resistance in tomato. Nat Biotechnol. 2018;36:1117.
pubmed: 30412196
doi: 10.1038/nbt1118-1117
Nishioka T, Marian M, Kobayashi I, Kobayashi Y, Yamamoto K, Tamaki H, et al. Microbial basis of Fusarium wilt suppression by Allium cultivation. Sci Rep. 2019;9:1715.
pubmed: 30737419
pmcid: 6368641
doi: 10.1038/s41598-018-37559-7
Johansen JE, Binnerup SJ. Contribution of Cytophaga-like bacteria to the potential turnover of carbon, nitrogen, and phosphorus by bacteria in the rhizosphere of barley (Hordeum vulgare L.). Microb Ecol. 2002;43:298–306.
pubmed: 12037608
doi: 10.1007/s00248-002-2006-z
Santos-Beneit F. The Pho regulon: a huge regulatory network in bacteria. Front Microbiol. 2015;6:402.
pubmed: 25983732
pmcid: 4415409
doi: 10.3389/fmicb.2015.00402
Antelmann H, Scharf C, Hecker M. Phosphate starvation-inducible proteins of Bacillus subtilis: proteomics and transcriptional analysis. J Bacteriol. 2000;182:4478–90.
pubmed: 10913081
pmcid: 94619
doi: 10.1128/JB.182.16.4478-4490.2000
Lidbury IDEA, Murphy ARJ, Scanlan DJ, Bending GD, Jones AME, Moore JD. et al. Comparative genomic, proteomic and exoproteomic analyses of three Pseudomonas strains reveals novel insights into the phosphorus scavenging capabilities of soil bacteria. Environ Microbiol. 2016;18:3535–49.
pubmed: 27233093
pmcid: 5082522
doi: 10.1111/1462-2920.13390
Zaheer R, Morton R, Proudfoot M, Yakunin A, Finan TM. Genetic and biochemical properties of an alkaline phosphatase PhoX family protein found in many bacteria. Environ Microbiol. 2009;11:1572–87.
pubmed: 19245529
doi: 10.1111/j.1462-2920.2009.01885.x
Bauer M, Kube M, Teeling H, Richter M, Lombardot T, Allers E, et al. Whole genome analysis of the marine Bacteroidetes ‘Gramella forsetii’ reveals adaptations to degradation of polymeric organic matter. Environ Microbiol. 2006;8:2201–13.
pubmed: 17107561
doi: 10.1111/j.1462-2920.2006.01152.x
Kolton M, Sela N, Elad Y, Cytryn E. Comparative genomic analysis indicates that niche adaptation of terrestrial flavobacteria is strongly linked to plant glycan metabolism. PLoS ONE. 2013;8:e76704.
pubmed: 24086761
pmcid: 3784431
doi: 10.1371/journal.pone.0076704
Martens EC, Koropatkin NM, Smith TJ, Gordon JI. Complex glycan catabolism by the human gut microbiota: the Bacteroidetes Sus-like paradigm. J Biol Chem. 2009;284:24673–7.
pubmed: 19553672
pmcid: 2757170
doi: 10.1074/jbc.R109.022848
Glenwright AJ, Pothula KR, Bhamidimarri SP, Chorev DS, Baslé A, Firbank SJ, et al. Structural basis for nutrient acquisition by dominant members of the human gut microbiota. Nature. 2017;541:407–11.
pubmed: 28077872
pmcid: 5497811
doi: 10.1038/nature20828
Foley MH, Cockburn DW, Koropatkin NM. The Sus operon: a model system for starch uptake by the human gut Bacteroidetes. Cell Mol Life Sci. 2016;73:2603–1.
pubmed: 27137179
pmcid: 4924478
doi: 10.1007/s00018-016-2242-x
Kappelmann L, Krüger K, Hehemann J-H, Harder J, Markert S, Unfried F, et al. Polysaccharide utilization loci of North Sea Flavobacteriia as basis for using SusC/D-protein expression for predicting major phytoplankton glycans. ISME J. 2019;13:76–91.
pubmed: 30111868
doi: 10.1038/s41396-018-0242-6
Zhu Y, Thomas F, Larocque R, Li N, Duffieux D, Cladière L, et al. Genetic analyses unravel the crucial role of a horizontally acquired alginate lyase for brown algal biomass degradation by Zobellia galactanivorans. Environ Microbiol. 2017;19:2164–81.
pubmed: 28205313
doi: 10.1111/1462-2920.13699
Cuskin F, Lowe EC, Temple MJ, Zhu Y, Cameron EA, Pudlo NA, et al. Human gut Bacteroidetes can utilize yeast mannan through a selfish mechanism. Nature 2015;517:165–9.
pubmed: 25567280
pmcid: 4978465
doi: 10.1038/nature13995
Larsbrink J, Zhu Y, Kharade SS, Kwiatkowski KJ, Eijsink VGH, Koropatkin NM, et al. A polysaccharide utilization locus from Flavobacterium johnsoniae enables conversion of recalcitrant chitin. Biotechnol Biofuels. 2016;9:2.
doi: 10.1186/s13068-016-0674-z
Cordell D, Drangert J-O, White S. The story of phosphorus: global food security and food for thought. Glob Environ Change. 2009;19:292–305.
doi: 10.1016/j.gloenvcha.2008.10.009
Tyrrell T. The relative influences of nitrogen and phosphorus on oceanic primary production. Nature 1999;400:525–31.
doi: 10.1038/22941
Filippelli GM. The global phosphorus cycle: past, present, and future. Elements. 2008;4:89–95.
doi: 10.2113/GSELEMENTS.4.2.89
Yang N, Zavišić A, Pena R, Polle A. Phenology, photosynthesis, and phosphorus in European beech (Fagus sylvatica L.) in two forest soils with contrasting P contents. J Plant Nutr Soil Sci. 2016;179:151–8.
doi: 10.1002/jpln.201500539
Goll DS, Brovkin V, Parida BR, Reick CH, Kattge J, Reich PB, et al. Nutrient limitation reduces land carbon uptake in simulations with a model of combined carbon, nitrogen and phosphorus cycling. Biogeosciences. 2012;9:3547–69.
doi: 10.5194/bg-9-3547-2012
Cordell D, White S. Tracking phosphorus security: indicators of phosphorus vulnerability in the global food system. Food Security. 2015;7:337–50.
doi: 10.1007/s12571-015-0442-0
White PJ, Hammond JP. Phosphorus nutrition of terrestrial plants. In: White PJ, Hammond JP, editors. The ecophysiology of plant-phosphorus interactions. Dordrecht: Springer Netherlands; 2008. p. 51–81.
Sharma SB, Sayyed RZ, Trivedi MH, Gobi TA. Phosphate solubilizing microbes: sustainable approach for managing phosphorus deficiency in agricultural soils. SpringerPlus. 2013;587.
Turner BL, Papházy MJ, Haygarth PM, McKelvie ID. Inositol phosphates in the environment. Philos Trans R Soc Lond B Biol Sci. 2002;357:449–69.
pubmed: 12028785
pmcid: 1692967
doi: 10.1098/rstb.2001.0837
Schachtman DP, Reid RJ, Ayling SM. Phosphorus uptake by plants: from soil to cell. Plant Physiol. 1998;116:447–53.
pubmed: 9490752
pmcid: 1539172
doi: 10.1104/pp.116.2.447
Zou X, Binkley D, Doxtader KG. A new method for estimating gross phosphorus mineralization and immobilization rates in soils. Plant Soil. 1992;147:243–50.
doi: 10.1007/BF00029076
Zoysa AKN, Loganathan P, Hedley MJ. A technique for studying rhizosphere processes in tree crops: soil phosphorus depletion around camellia (Camellia japonica L.) roots. Plant Soil. 1997;190:253–65.
doi: 10.1023/A:1004264830936
Shen J, Yuan L, Zhang J, Li H, Bai Z, Chen X, et al. Phosphorus dynamics: from soil to plant. Plant Physiol. 2011;156:997–1005.
pubmed: 21571668
pmcid: 3135930
doi: 10.1104/pp.111.175232
Stutter MI, Shand CA, George TS, Blackwell MSA, Bol R, MacKay RL, et al. Recovering phosphorus from soil: a root solution? Environ Sci Technol. 2012;46:1977–8.
pubmed: 22280364
doi: 10.1021/es2044745
Wanner BL. Phosphorus assimilation and its control of gene expression in Escherichia coli. In: Hauska G, Thauer R, editors. The molecular basis of bacterial metabolism. Colloquium der Gesellschaft für Biologische Chemie 5.–7.1990. Mosbach/Baden: Springer Berlin Heidelberg; 1990. p. 152–63.
Gandhi NU, Chandra SB A comparative analysis of three classes of bacterial non-specific acid phosphatases and archaeal phosphoesterases: evolutionary perspective. Acta Inform Med. 2012;20:167–73.
doi: 10.5455/aim.2012.20.167-173
IDEA Lidbury, Fraser T, Murphy ARJ, Scanlan DJ, Bending GD, AME Jones, et al. The ‘known’ genetic potential for microbial communities to degrade organic phosphorus is reduced in low-pH soils. Microbiol Open. 2017;6:e00474.
doi: 10.1002/mbo3.474
Kolton M, Green SJ, Harel YM, Sela N, Elad Y, Cytryn E. Draft genome sequence of Flavobacterium sp. strain F52, isolated from the rhizosphere of Bell Pepper (Capsicum annuum L. cv. Maccabi). J Bacteriol. 2012;194:5462–3.
pubmed: 22965088
pmcid: 3457196
doi: 10.1128/JB.01249-12
McBride MJ, Kempf MJ. Development of techniques for the genetic manipulation of the gliding bacterium Cytophaga johnsonae. J Bacteriol. 1996;178:583–90.
pubmed: 8550486
pmcid: 177698
doi: 10.1128/jb.178.3.583-590.1996
Nishioka T, Elsharkawy MM, Suga H, Kageyama K, Hyakumachi M, Shimizu M. Development of culture medium for the isolation of Flavobacterium and Chryseobacterium from rhizosphere soil. Microbes Environ. 2016;31:104–10.
pubmed: 27098502
pmcid: 4912144
doi: 10.1264/jsme2.ME15144
Gil R, Silva FJ, Peretó J, Moya A. Determination of the core of a minimal bacterial gene set. Microbiol Mol Biol Rev. 2004;68:518–37.
pubmed: 15353568
pmcid: 515251
doi: 10.1128/MMBR.68.3.518-537.2004
Seemann T. Prokka: rapid prokaryotic genome annotation. Bioinformatics 2014;30:2068–9.
pubmed: 24642063
doi: 10.1093/bioinformatics/btu153
Minh BQ, Schmidt HA, Chernomor O, Schrempf D, Woodhams MD, von Haeseler A, et al. IQ-TREE 2: New models and efficient methods for phylogenetic inference in the genomic era. Mol Biol Evol. 2020;37:1530–4.
pubmed: 32011700
pmcid: 7182206
doi: 10.1093/molbev/msaa015
Roca A, Pizarro-Tobías P, Udaondo Z, Fernández M, Matilla MA, Molina-Henares MA, et al. Analysis of the plant growth-promoting properties encoded by the genome of the rhizobacterium Pseudomonas putida BIRD-1. Environ Microbiol. 2013;15:780–94.
pubmed: 23206161
doi: 10.1111/1462-2920.12037
IDEA Lidbury, Murphy ARJ, Fraser TD, et al. Identification of extracellular glycerophosphodiesterases in Pseudomonas and their role in soil organic phosphorus remineralisation. Sci Rep. 2017;7:2179. JD, et al.
doi: 10.1038/s41598-017-02327-6
Brickman E, Beckwith J. Analysis of the regulation of Escherichia coli alkaline phosphatase synthesis using deletions and φ80 transducing phages. J Mol Biol. 1975;96:307–15.
pubmed: 1100846
doi: 10.1016/0022-2836(75)90350-2
Skouri-Panet F, Benzerara K, Cosmidis J, Férard C, Caumes G, De Luca G, et al. In vitro and in silico evidence of phosphatase diversity in the biomineralizing bacterium Ramlibacter tataouinensis. Front Microbiol. 2018;8:2592.
pubmed: 29375498
pmcid: 5768637
doi: 10.3389/fmicb.2017.02592
Berlutti F, Passariello C, Selan L, Thaller MC, Rossolini GM. The Chryseobacterium meningosepticum PafA enzyme: prototype of a new enzyme family of prokaryotic phosphate-irrepressible alkaline phosphatases? Microbiology. 2001;147:2831–9.
pubmed: 11577161
doi: 10.1099/00221287-147-10-2831
Lombard V, Golaconda Ramulu H, Drula E, Coutinho PM, Henrissat B. The carbohydrate-active enzymes database (CAZy) in 2013. Nucleic Acids Res. 2014;42:D490–5.
pubmed: 24270786
doi: 10.1093/nar/gkt1178
Sunden F, AlSadhan I, Lyubimov AY, Ressl S, Wiersma-Koch H, Borland J, et al. Mechanistic and evolutionary insights from comparative enzymology of phosphomonoesterases and phosphodiesterases across the alkaline phosphatase superfamily. J Am Chem Soc. 2016;138:14273–87.
pubmed: 27670607
pmcid: 5096464
doi: 10.1021/jacs.6b06186
Le Blastier S, Hamels A, Cabeen M, Schille L, Tilquin F, Dieu M, et al. Phosphate starvation triggers production and secretion of an extracellular lipoprotein in Caulobacter crescentus. PLoS ONE. 2010;5:e14198.
pubmed: 21152032
pmcid: 2996285
doi: 10.1371/journal.pone.0014198
Maldonado MC, Strasser, de Saad AM. Production of pectinesterase and polygalacturonase by Aspergillus niger in submerged and solid state systems. J Ind Microbiol Biotechnol. 1998;20:34–8.
pubmed: 9523455
doi: 10.1038/sj.jim.2900470
Bolam DN, van den Berg B. TonB-dependent transport by the gut microbiota: novel aspects of an old problem. Curr Opin Struct Biol. 2018;51:35–43.
pubmed: 29550504
doi: 10.1016/j.sbi.2018.03.001
Haygarth PM, Harrison AF, Turner BL. On the history and future of soil organic phosphorus research: a critique across three generations. Eur J Soil Sci. 2018;69:1.
doi: 10.1111/ejss.12517
Putker F, Tommassen-van Boxtel R, Stork m, Rodríguez-Herva JJ, Koster M, Tommassen J. The type II secretion system (Xcp) of Pseudomonas putida is active and involved in the secretion of phosphatases. Environ Microbiol. 2013;15:2658–71.
pubmed: 23530902
Yong SC, Roversi P, Lillington J, Rodriguez F, Krehenbrink M, Zeldin OB, et al. A complex iron-calcium cofactor catalyzing phosphotransfer chemistry. Science. 2014;345:1170–3.
pubmed: 25190793
pmcid: 4175392
doi: 10.1126/science.1254237
Joglekar P, Sonnenburg ED, Higginbottom SK, Earle KA, Morland C, Shapiro-Ward S, et al. Genetic variation of the SusC/SusD homologs from a polysaccharide utilization locus underlies divergent fructan specificities and functional adaptation in Bacteroides thetaiotaomicron. mSphere. 2018;3:e00185–18.
pubmed: 29794055
pmcid: 5967196
doi: 10.1128/mSphereDirect.00185-18
Lim BL, Yeung P, Cheng C, Hill JE. Distribution and diversity of phytate-mineralizing bacteria. ISME J. 2007;1:321–30.
pubmed: 18043643
doi: 10.1038/ismej.2007.40
Zhu XF, Wang ZW, Wan JX, Sun Y, Wu YR, Li GX, et al. Pectin enhances rice (Oryza sativa) root phosphorus remobilization. J Exp Bot. 2014;66:1017–24.
pubmed: 25528599
doi: 10.1093/jxb/eru461
Reintjes G, Arnosti C, Fuchs BM, Amann R. An alternative polysaccharide uptake mechanism of marine bacteria. ISME J. 2017;11:1640–50.
pubmed: 28323277
pmcid: 5520146
doi: 10.1038/ismej.2017.26
Turner BL, Haygarth PM. Phosphatase activity in temperate pasture soils: Potential regulation of labile organic phosphorus turnover by phosphodiesterase activity. Sci Total Environ. 2005;344:27–36.
pubmed: 15907508
doi: 10.1016/j.scitotenv.2005.02.003
Sergaki C, Lagunas B, Lidbury I, Gifford ML, Schäfer P. Challenges and approaches in microbiome research: From fundamental to applied. Front Plant Sci. 2018;9:1205.
pubmed: 30174681
pmcid: 6107787
doi: 10.3389/fpls.2018.01205