Enhanced mutualism: A promotional effect driven by bacteria during the early invasion of Phytolacca americana

Abstract

The enhanced mutualism hypothesis postulates that invasive plants promote self‐growth by enriching beneficial microbes to establish a positive soil feedback. However, the roles of soil microorganisms may vary with increasing time for plant growth. Research on changes in soil microbial communities over time has important implications for understanding the mechanisms underlying plant invasion. Due to the difficulty in evaluating the duration of plant growth, few studies have quantified the changes in soil microorganisms with increasing plant age. This study focuses on the invasive weed Phytolacca americana L., which has growth rings in the main root. We conducted a two‐stage experiment in the field and greenhouse to explore the soil feedback changes with duration of plant growth. We determined the effects of P. americana at different ages on the soil microbial community and soil properties and performed a soil inoculation experiment to quantify the influence of soil microbes on seed germination and seedling performance. We found that the content of some soil nutrients, namely total nitrogen, total phosphorus, nitrate‐N, and available phosphorus, significantly decreased with increasing growth age of P. americana, whereas the available potassium showed an opposite increasing trend. The P. americana growth age also significantly influenced the soil bacterial community structure. However, this phenomenon did not occur in the fungal community. In the bacterial community, the relative abundance of plant growth‐promoting bacteria showed an increasing trend. The soil inoculation experiment had high seed germination rates and biomass accumulation when the plants were grown in conditioned soil from P. americana growth within 5 years, suggesting a positive plant–soil feedback. However, the promoting effect disappeared in conditioned soil from 10 years of age. Our findings demonstrate that plant growth‐promoting bacteria significantly accumulated in the soil during the early stages of P. americana invasion, and that the strength of enhanced positive feedback may play a crucial role in facilitating P. americana invasion. This study highlights the changing nature of plant–microbe interactions during biological invasion and illustrates how bacteria could contribute to the initial success of P. americana, providing new insights into the underlying mechanisms of plant invasion.

Exotic plantations differ in “nursing” an understory invader: A probe into invasional meltdown

“…Initial invaders may promote the secondary invasion of subsequent species by facilitating mutualism (Meng et al., 2024; Zhang et al., 2020), gathering pathogenic fungi (Inderjit & van der Putten, 2010), and destroying the native mycorrhizal system and facilitating mutualistic integration (Hale et al., 2011; Stinson et al., 2006). Considering the soil bacteria, P. americana “gathered” a greater abundance of Streptomyces in the understory of R. pseudoacacia stand.…”

Perspectives of invasive alien species management in China

“…Conversely, the enhanced mutualism hypothesis posits that invasive plants promote their own growth by enriching beneficial microbes in the soil, thereby establishing positive soil feedback. Meng et al (2023) found that plant growth‐promoting bacteria accumulated significantly in the soil during the early stages of Phytolacca americana invasions, and in turn the strength of enhanced positive feedback was likely to have facilitated P. americana invasions. This study highlights the evolving nature of plant–microbe interactions during biological invasions and underscores the role of bacteria in the initial success of P. americana invasions.…”

Plant G x Microbial E: Plant genotype interaction with soil bacterial community shapes rhizosphere composition during invasion

“…Invaders could also benefit from differences in plant-soil feedbacks that accumulate over time (Levine et al 2006). Plants experience negative feedbacks when a host-specific pathogen accumulates in the soil and suppresses their growth (Bever 2003, 2002), or positive feedbacks if the same dynamic occurs with a mutualist (Uddin et al 2021), and invading species have been observed to benefit from enhanced positive or reduced negative feedbacks in soils from their introduced ranges (Uddin et al 2021; Maron et al 2014; McGinn et al 2018; Meng et al 2024; Suding et al 2013; van der Putten et al 2013). Invaders might also benefit from interactions with a simplified microbial interaction network in a novel environment, allowing invaders to be more efficient in exploiting mutualists or defending against pathogens (Colautti and Lau 2015; Mesa and Dlugosch 2020).…”