Prime time for Paraburkholderia – agents of soil priming

Written by: Roland C. Wilhelm and Daniel H. Buckley

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Bacteria have a way of hiding in plain sight, their importance masked by their invisibility and often nondescript appearance. Paraburkholderia are an odd case – they have been studied for decades under different names, like Pseudomonas or Burkholderia, until a recent phylogenomic analysis revealed their hidden identity [1]. Now that we recognize Paraburkholderia, we can finally give them the attention they deserve. Paraburkholderia are abundant and widespread in soil and are extraordinarily versatile in function, possessing large multi-replicon genomes [2]. Some protect plants from pathogens, others enhance plant growth by fixing nitrogen and solubilizing phosphate minerals [3–5], and most are champions at degrading aromatic compounds produced by plants [6–8], fungi [9], and humans [10, 11]. We found that Paraburkholderia can also facilitate a phenomenon called ‘soil priming’, which we believe has important consequences for soil carbon cycling [12].


Fig. 1 - An illustration of the soil priming effect.
Fig. 1. An illustration of the soil priming effect.

          We set out to identify phenolic-acid degrading bacteria in forest soils and to evaluate their role in soil priming. Priming occurs when new carbon added to soil stimulates the mineralization of existing carbon stores (Fig. 1). Prior research has shown that phenolics and aromatics could reliably produce soil priming [8, 13], but what caused this effect was unknown. We found that populations of Paraburkholderia were chiefly responsible. We characterized one of the most active species, Paraburkholderia madseniana [14], and named it in honor of our late co-author Dr. Eugene Madsen who initiated our efforts (Fig. 2). P. madseniana is a fast-growing organism that is equipped with diverse and numerous pathways for degrading aromatics. Populations of P. madseniana grew rapidly when either glucose or phenolic acids were added to soil, but priming was specifically induced in the presence of phenolics. Thus, we concluded that Paraburkholderia, and their specialized capacity to degrade phenolics and aromatics, are prime-time players in soil carbon cycling.


Fig. 2. Photograph of Dr. Eugene Madsen after whom a new
species of Paraburkholderia was named.

          One of our most interesting observations relates to their potential partnership with plant roots. Our study was conducted in a long-term experimental forest, a common garden experiment with different tree species. We observed that the highest phenolic-degrading activity was associated with sugar maple, which had densely matted roots, and coincided with lower-than-average soil carbon stores. In contrast, soils in black locust plantations, a leguminous tree that can form nodules containing Paraburkholderia, had far fewer roots and higher levels of soil carbon. From this, we hypothesized that soil priming by roots can be driven by the exudation of phenolic acids which enhance the activity of Paraburkholderia to degrade soil organic matter, thereby releasing nutrients that promote plant growth (Fig. 3). We suspect that Paraburkholderia form associations with a diversity of plants and that they are key players in regulating soil priming phenomena that influence plant growth dynamics and drive the fate of soil carbon.


Fig. 3. A conceptual framework illustrating how phenolic acid-degrading bacteria can prime elemental cycling in soils. In this framework, plant roots gain access to N and P stored in soil organic matter (SOM) by stimulating the growth and inducing the activity of phenolic acid-degrading bacteria to secrete extracellular oxidative enzymes (EOEs). The full framework is provided in Fig. 7 in our open access article.

References

  1. Sawana A, Adeolu M, Gupta RS, Nierman WC, Craig J. Molecular signatures and phylogenomic analysis of the genus Burkholderia: Proposal for division of this genus into the emended genus Burkholderia containing pathogenic organisms and a new genus Paraburkholderia gen. nov. harboring env. Front Genet 2014; 5: 1–22. (link)
  2. Chain PSG, Denef VJ, Konstantinidis KT, Vergez LM, Agulló L, VL R, et al. Burkholderia xenovorans LB400 harbors a multi-replicon, 9.73-Mbp genome shaped for versatility. Proc Natl Acad Sci 2006; 103: 15280–15287. (link)
  3. Esmaeel Q, Miotto L, Rondeau M, Leclère V, Charles TC. Paraburkholderia phytofirmans PsJN-Plants Interaction : From Perception to the Induced Mechanisms. 2018; 9: 1–14. (link)
  4. Andreolli M, Lampis S, Poli M, Gullner G, Biró B, Vallini G. Endophytic Burkholderia fungorum DBT1 can improve phytoremediation efficiency of polycyclic aromatic hydrocarbons. Chemosphere 2013; 92: 688–694. (link)
  5. Aziz MZ, Yaseen M, Naveed M, Wang X, Fatima K, Saeed Q, et al. Polymer-Paraburkholderia phytofirmans PsJN Coated Survival, Phosphorous Use Efficiency, and Production of Wheat. Agronomy 2020; 10. (link)
  6. Badri D V., Chaparro JM, Zhang R, Shen Q, Vivanco JM. Application of natural blends of phytochemicals derived from the root exudates of Arabidopsis to the soil reveal that phenolic-related compounds predominantly modulate the soil microbiome. J Biol Chem 2013; 288: 4502–4512. (link)
  7. Zhalnina K, Louie KB, Hao Z, Mansoori N, da Rocha UN, Shi S, et al. Dynamic root exudate chemistry and microbial substrate preferences drive patterns in rhizosphere microbial community assembly. Nat Microbiol 2018; 3: 1–11. (link)
  8. Zwetsloot MJ, Muñoz Ucros J, Wickings K, Wilhelm RC, Sparks JP, Buckley DH, et al. Prevalent root-derived phenolics drive shifts in microbial community composition and prime decomposition in forest soil. Soil Biol Biochem 2020; 145. (link)
  9. Coenye T, Laevens S, Willems A, Ohlen M, Hannant W, Govan JRW, et al. . Burkholderia fungorum sp. nov. and Burkholderia caledonica sp. nov., two new species isolated from the environment, animals and human clinical samples. Int J Syst Evol Microbiol 2001; 51: 1099–1107. (link)
  10. Fulthorpe R, Dunbar J, Holben B, Forney L, Maltseva O, Matheson G, et al. 2,4-Dichlorophenoxyacetate Degraders in the Real World, Do We Know Who They Are? JRDC-MSU Jt Work Microb Evol Biodegrad 1994. (link)
  11. Goris J, De Vos P, Caballero-Mellado J, Park J, Falsen E, Quensen JF, et al. Classification of the biphenyl- and polychlorinated biphenyl-degrading strain LB400T and relatives as Burkholderia xenovorans sp. nov. Int J Syst Evol Microbiol 2004; 54: 1677–1681. (link)
  12. Wilhelm RC*, DeRito CM*, Shapleigh JP, Buckley DH, Madsen EL. Phenolic acid-degrading Paraburkholderia prime decomposition in forest soil. ISME Commun 2021. (link)
  13. Lonardo DP Di, Boer W De, Gunnewiek PJAK, Hannula SE, Wal A Van Der. Soil Biology & Biochemistry Priming of soil organic matter : Chemical structure of added compounds is more important than the energy content. 2017; 108. (link)
  14. Wilhelm RC, Murphy SJLL, Feriancek NM, Karasz DC, Derito CM, Newman D, et al. Paraburkholderia madseniana sp. nov., a phenolic acid-degrading bacterium isolated from acidic forest soil. Int J Syst Evol Microbiol 2020; 70: 2137–2146. (link)

Roland C. Wilhelm

Postdoctoral Researcher, Cornell University