Introduced Streptomyces pactum increases indigenous Pseudomonas koreensis population in the rhizosphere by enhancing chemotaxis and biofilm formation

Beneficial microbes can be used as biocontrol agents against soil-borne plant diseases. In addition to controlling plant pathogens and promoting plant growth, an introduced biocontrol agent also plays a role in shifting the indigenous microbial community structure in the rhizosphere. However, it remains unclear how biocontrol agents affect the distribution of rhizosphere microbial populations and whether the population change of particular dominant microbes in turn contributes to the role of the biocontrol agent in disease control and plant growth promotion. Our previous studies indicated that introduction of Streptomyces pactum Act12 (a multifunctional biocontrol agent) could regulate rhizosphere microecology and, particularly, increase the population of Pseudomonas koreensis GS (a dominant indigenous bacterium) in the ginseng rhizosphere. Herein, we evaluated the potential effects of P. koreensis GS in disease control and plant growth promotion via in vitro antagonism and tomato seedling growth tests. We found that P. koreensis GS had no antagonistic effect on six common fungal pathogens. Nonetheless, seed priming with cell-free culture filtrate of strain GS considerably promoted tomato seedling growth in terms of hypocotyl and radicle length as well as expandin gene expression in leaves compared with controls. Then, we explored the molecular mechanisms underpinning the population increase of P. koreensis GS after S. pactum Act12 treatment based on growth and transcriptome changes of strain GS. We found that adding broth culture, cell-free filtrate, or spore powder of S. pactum Act12 did not significantly affect P. koreensis GS growth in solid agar, liquid broth, or sterilized soil, respectively. Nonetheless, RNA sequencing revealed that organic acid and reactive oxygen species metabolic processes were upregulated, while expression levels of genes involved in bacterial chemotaxis and flagellar assembly were increased in the Act12 treatment group compared with the control group. Colonization-related phenotype analysis showed that S. pactum Act12 treatment also improved the swimming motility of, and biofilm formation by, P. koreensis GS. These results indicate that introduction of S. pactum Act12 can improve the rhizosphere colonization and competition abilities of P. koreensis GS via the enhancement of biofilm formation, nutrient use, and environmental adaptability. The resulting increase in the P. koreensis population may directly contribute to the role of S. pactum Act12 in promotion of plant growth.