Abstract
In this study, we explore variation in resource use among Streptomyces in prairie soils. Resource use patterns were highly variable among Streptomyces isolates and were significantly related to location, phylogeny, and nitrogen (N) amendment history. Streptomyces populations from soils less than 1 m apart differed significantly in their ability to use resources, indicating that drivers of resource use phenotypes in soil are highly localized. Variation in resource use within Streptomyces genetic groups was significantly associated with the location from which Streptomyces were isolated, suggesting that resource use is adapted to local environments. Streptomyces from soils under long-term N amendment used fewer resources and grew less efficiently than those from non-amended soils, demonstrating that N amendment selects for Streptomyces with more limited catabolic capacities. Finally, resource use among Streptomyces populations was correlated with soil carbon content and Streptomyces population densities. We hypothesize that variation in resource use among Streptomyces reflects adaptation to local resource availability and competitive species interactions in soil and that N amendments alter selection for resource use phenotypes.
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Tilman D (1982) Resource competition and community structure, Monogr Pop Biol 17. Princeton University Press, Princeton
Loreau M, Hector A (2001) Partitioning selection and complementarity in biodiversity experiments. Nature 412:72–76
Tilman D (2004) Niche tradeoffs, neutrality, and community structure: a stochastic theory of resource competition, invasion, and community assembly. Proc Natl Acad Sci U S A 101:10854–10861
Barrett RDH, Craig MacLean R, Bell G (2005) Experimental evolution of Pseudomonas fluorescens in simple and complex environments. Am Nat 166:470–480
Schlatter D, Fubuh A, Xiao K, Hernandez D, Hobbie S, Kinkel L (2009) Resource amendments influence density and competitive phenotypes of Streptomyces in soil. Microb Ecol 57:413–420
Folman LB, Postma J, Veen JA (2001) Ecophysiological characterization of rhizosphere bacterial communities at different root locations and plant developmental stages of cucumber grown on rockwool. Microb Ecol 42:586–597
Craig MacLean R, Dickson A, Bell G (2005) Resource competition and adaptive radiation in a microbial microcosm. Ecol Letters 8:38–46
Lawrence D, Fiegna F, Behrends V, Bundy JG, Phillimore AB, Bell T, Barraclough TG (2012) Species interactions alter evolutionary responses to a novel environment. PLoS Biol 10(5):e1001330
Garbeva P, van Veen JA, van Elsas JD (2004) Microbial diversity in soil: selection of microbial populations by plant and soil type and implications for disease suppressiveness. Annu Rev Phytopathol 42:243–270
Fierer N, Bradford MA, Jackson RB (2007) Toward and ecological classification of soil bacteria. Ecology 88:1354–1364
Wiggins BE, Kinkel LL (2005) Green manures and crop sequences influence alfalfa root rot and pathogen inhibitory activity among soil-borne streptomycetes. Plant Soil 286:271–283
Wiggins BE, Kinkel LL (2005) Green manures and crop sequences influence potato diseases and pathogen inhibitory activity of indigenous streptomycetes. Phytopathol 95:178–185
Clardy J, Fischbach MA, Walsh CT (2006) New antibiotics from bacterial natural products. Nature Biotechnol 24:1541–1550
Hodgson DA (2000) Primary metabolism and its control in streptomycetes: a most unusual group of bacteria. Adv Microb Physiol 42:47–238
Williamson N, Brian P, Wellington EMH (2000) Molecular detection of bacterial and streptomycete chitinases in the environment. Antonie van Leeuwenhoek 78:315–321
Chater KF, Biró S, Lee KJ, Palmer T, Schrempf H (2010) The complex extracellular biology of Streptomyces. FEMS Microbiol Rev 34:171–198
Schrempf H, Koebsch I, Walter S, Engelhardt H, Meschke H (2011) Extracellular Streptomyces vesicles: amphorae for survival and defence. Microb Biotechnol 4:286–299
Seipke RF, Kaltenpoth M, Hutchings MI (2011) Streptomyces as symbionts: an emerging and widespread theme? FEMS Microbiol Rev 36:862–876
Kinkel LL, Schlatter DC, Bakker MG, Arenz BE (2012) Streptomyces competition and co-evolution in relation to disease suppression. Res Microbiol 163:490–499
Williams ST, Vickers JC (1986) The ecology of antibiotic production. Microb Ecol 12:43–52
Slattery M, Pajbhandari K, Wesson K (2001) Competition-mediated antibiotic induction in the marine bacterium Streptomyces tenjimariensis. Microb Ecol 41:90–96
Davelos AL, Kinkel LL, Samac DA (2004) Spatial variation in frequency and intensity of antibiotic interactions among streptomycetes from prairie soil. Appl Environ Microbiol 70:1051–1058
Rigali S, Titgemeyer F, Barends S, Mulder S, Thomae AW, Hopwood DA, van Wezel GP (2008) Feast or famine: the global regulator DasR links resource stress to antibiotic production by Streptomyces. EMBO Reports 9:670–675
Sánchez S, Chávez A, Forero A, García-Huante Y, Romero A, Sánchez M, Rocha D, Sánchez B, Avalos M, Guzmán-Trampe S, Rodríguez-Sanoja R, Langley E, Ruiz B (2010) Carbon source regulation of antibiotic production. J Antibiot 63:442–459
Frey SD, Knorr M, Parrent JL, Simpson RT (2004) Chronic nitrogen enrichment affects the structure and function of the soil microbial community in temperate hardwood and pine forests. Forest Ecol Man 196:159–171
Knorr M, Frey SD, Curtis PS (2005) Nitrogen additions and litter decomposition: a meta-analysis. Ecology 86:3252–3257
Eisenlord SD, Zak DR (2010) Simulated atmospheric nitrogen deposition alters Actinobacterial community composition in forest soils. Soil Biol Biochem 74:1157–1166
Ramirez KS, Lauber CL, Knight R, Bradford MA, Fierer N (2010) Consistent effects of nitrogen fertilization on soil bacterial communities in contrasting systems. Ecology 91:3563–3470
Fierer N, Lauber CL, Ramirez KS, Zaneveld J, Bradford MA, Knight R (2012) Comparative metagenomic, phylogenetic and physiological analyses of soil microbial communities across nitrogen gradients. ISME J 6:1007–1017
Ramirez KS, Craine JM, Fierer N (2012) Consistent effects of nitrogen amendments on soil microbial communities and processes across biomes. Global Change Biol 18:1918–1927
Carreiro MM, Sinsabaugh RL, Repert DA, Parkhurst DF (2000) Microbial enzyme shifts explain litter decay responses to simulated nitrogen deposition. Ecology 81:2359–2365
Gallo M, Amonette R, Lauber C, Sinsabaugh RL, Zak DR (2004) Microbial community structure and oxidative enzyme activity in nitrogen-amended north temperate forest soils. Microb Ecol 48:218–229
Otto-Hanson LK, Grabau Z, Rosen C, Salomon CE, Kinkel LL (2013) Pathogen variation and urea influence selection and success of Streptomyces mixtures in biocontrol. Phytopathol 103:34–42
Clark CM, Tilman D (2008) Loss of plant species after chronic low-level nitrogen deposition to prairie grasslands. Nature 451:712–715
Davelos AL, Xiao K, Samac DA, Martin AP, Kinkel LL (2004) Spatial variation in Streptomyces genetic composition and diversity in a prairie soil. Microb Ecol 48:601–612
Takeuchi T, Sawada H, Tanaka F, Matsuda I (1996) Phylogenetic analysis of Streptomyces spp. causing potato scab based on 16S rRNA sequences. Int J Syst Bacteriol 46:467–469
Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98
Oksanen J, Blanchet G, Kindt R, Legendre P, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Stevens MHH, Wagner H (2011) vegan: community ecology package. R package version 2.0-2. http://CRAN.R-project.org/package=vegan
R Development Core Team (2011) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. http://www.R-project.org/
Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB et al (2009) Introducing mother: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541
Langenheder S, Székely AJ (2011) Species sorting and neutral processes are both important during the initial assembly of bacterial communities. ISME J 5:1086–1094
Kassen R (2002) The experimental evolution of specialists, generalists, and the maintenance of diversity. J Evol Biol 15:173–190
Antony-Babu S, Stach JEM, Goodfellow M (2008) Genetic and phenotypic evidence for Streptomyces griseus ecovars isolated from a beach and dune sand system. Antonie van Leeuwenhoek 94:63–74
Aldén L, Demoling F, Bååth E (2001) Rapid method of determining factors limiting bacterial growth in soil. Appl Environ Microbiol 67:1830–1838
Kassen R, Rainey PB (2004) The ecology and genetics of microbial diversity. Annu Rev Microbiol 58:207–231
Czárán T, Hoekstra RF, Pagie L (2002) Chemical warfare between microbes promotes biodiversity. Proc Natl Acad Sci U S A 99:786–790
Hibbing ME, Fuqua C, Parsek MR, Peterson SB (2010) Bacterial competition: surviving and thriving in the microbial jungle. Nat Rev Microbiol 8:15–25
Garbeva P, Tyc O, Remus-Emsermann MNP, van der Wal A, Vos M, Silby M, de Boer W (2011) No apparent costs for facultative antibiotic production by the soil bacterium Pseudomonas fluorescens Pf0-1. PLoS One 6:e27266
Lopez-Pascua LDC, Buckling A (2008) Increasing productivity accelerates host–parasite coevolution. J Evol Biol 21:853–860
Wloch-Salomon DM, Gerla D, Hoekstra RF, de Visser JAG (2008) Effect of dispersal and resource availability on the competitive ability of toxin-producing yeast. Proc Royal Soc B: Biol Sci 275:535–541
Lopez-Pascua LDC, Brockhurst MA, Buckling A (2010) Antagonistic coevolution across productivity gradients: an experimental test of the effects of dispersal. J Evol Biol 23:207–211
Cohen MF, Mazzola M (2006) Resident bacteria, nitric oxide emission and particle size modulate the effect of Brassica napus seed meal on disease incited by Rhizoctonia solani and Pythium spp. Plant Soil 286:75–86
Mazzola M, Zhao X (2010) Brassica juncea seed meal particle size influences chemistry but not soil biology-based suppression of individual agents inciting apple replant disease. Plant Soil 337:313–324
Lenc L, Kwasna H, Sadowski C (2011) Dynamics of the root/soil pathogens and antagonists in organic and integrated production of potato. Eur J Plant Pathol 131:603–620
Kinkel LL, Bakker MG, Schlatter DC (2011) A coevolutionary framework for managing disease-suppressive soils. Annu Rev Phytopathol 49:47–67
Bakker MG, Bradeen JM, Kinkel LL (2013) Effects of plant host species and plant community richness on streptomycete community structure. FEMS Microbiol Ecol 83:596–606
Bulgarelli D, Schlaeppi K, Spaepen S, van Themaat EVL, Schulze-Lefert P (2013) Structure and functions of the bacterial microbiota of plants. Annu Rev Plant Biol 64:807–838
De Deyn GB, Quirk H, Bardgett RD (2011) Plant species richness, identity and productivity differentially influence key groups of microbes in grassland soils of contrasting fertility. Biol Lett 7(1):75–78. doi:10.1098/rsbl.2010.0575
Tilman D (1987) Secondary succession and the pattern of plant dominance along experimental nitrogen gradients. Ecol Monogr 57:189–214
Craine JM, Morrow C, Fierer N (2007) Microbial nitrogen limitation increases decomposition. Ecology 88:2105–2113
Meier CL, Bowman WD (2008) Links between plant litter chemistry, species diversity, and below-ground ecosystem function. Proc Natl Acad Sci U S A 105:19780–19785
Fontaine S, Mariotti A, Abbadie L (2003) The priming effect of organic matter: a question of microbial competition? Soil Biol Biochem 35:837–843
Acknowledgments
Support for this research was provided by the National Science Foundation Microbial Observatories Project 9977907, United States Department of Agriculture Microbial Observatories Program Grant 2006-35319-17445, and the Minnesota Agricultural Experiment Station MIN-22-018.
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Schlatter, D.C., DavelosBaines, A.L., Xiao, K. et al. Resource Use of Soilborne Streptomyces Varies with Location, Phylogeny, and Nitrogen Amendment. Microb Ecol 66, 961–971 (2013). https://doi.org/10.1007/s00248-013-0280-6
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DOI: https://doi.org/10.1007/s00248-013-0280-6