The biocontrol agent Streptomyces pactum increases Pseudomonas koreensis populations in the rhizosphere by enhancing chemotaxis and biofilm formation

Abstract

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 can cause shifts in the indigenous microbial community structure in the rhizosphere. However, it remains unclear how biocontrol agents affect the distribution of rhizosphere microbial populations and whether population changes of particular dominant microbes in turn contribute 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 affect rhizosphere micro-ecology and, particularly, increase the population of Pseudomonas koreensis GS (a dominant indigenous bacterium) in the rhizosphere of ginseng plants. Here 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. However, seed priming with cell-free culture filtrate of strain GS considerably promoted hypocotyl and radicle growth of tomato seedlings while increasing expression of expansin genes in seedling leaves compared with controls. Then, we explored the molecular mechanisms underpinning the population increase of P. koreensis GS based on its growth and transcriptome changes. 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 autoclaved soil, respectively. However, RNA sequencing revealed upregulation of genes related to organic acid metabolic processes, reactive oxygen species metabolic processes, bacterial chemotaxis, and flagellar assembly in P. koreensis GS after treatment with S. pactum Act12 cell-free filtrate. S. pactum Act12 treatment improved the swimming motility of, and biofilm formation by, P. koreensis GS, thereby enhancing its ability to colonize the rhizosphere of tomato seedlings. These results indicate that introduction of S. pactum Act12 can enhance rhizosphere colonization and competition by P. koreensis GS via the promotion of biofilm formation, nutrient utilization, and environmental adaptation. The resulting increase in the P. koreensis population may directly contribute to the role of S. pactum Act12 in promoting plant growth.