Stochastic Inoculum, Biotic Filtering and Species-Specific Seed Transmission Shape the Rare Microbiome of Plants

Abstract

A plant’s health and productivity is influenced by its associated microbes. Although the common/core microbiome is often thought to be the most influential, significant numbers of rare or uncommon microbes (e.g., specialized endosymbionts) may also play an important role in the health and productivity of certain plants in certain environments. To help identify rare/specialized bacteria and fungi in the most important angiosperm plants, we contrasted microbiomes of the seeds, spermospheres, shoots, roots and rhizospheres of Arabidopsis, Brachypodium, maize, wheat, sugarcane, rice, tomato, coffee, common bean, cassava, soybean, switchgrass, sunflower, Brachiaria, barley, sorghum and pea. Plants were grown inside sealed jars on sterile sand or farm soil. Seeds and spermospheres contained some uncommon bacteria and many fungi, suggesting at least some of the rare microbiome is vertically transmitted. About 95% and 86% of fungal and bacterial diversity inside plants was uncommon; however, judging by read abundance, uncommon fungal cells are about half of the mycobiome, while uncommon bacterial cells make up less than 11% of the microbiome. Uncommon-seed-transmitted microbiomes consisted mostly of Proteobacteria, Firmicutes, Bacteriodetes, Ascomycetes and Basidiomycetes, which most heavily colonized shoots, to a lesser extent roots, and least of all, rhizospheres. Soil served as a more diverse source of rare microbes than seeds, replacing or excluding the majority of the uncommon-seed-transmitted microbiome. With the rarest microbes, their colonization pattern could either be the result of stringent biotic filtering by most plants, or uneven/stochastic inoculum distribution in seeds or soil. Several strong plant–microbe associations were observed, such as seed transmission to shoots, roots and/or rhizospheres of Sarocladium zeae (maize), Penicillium (pea and Phaseolus), and Curvularia (sugarcane), while robust bacterial colonization from cassava field soil occurred with the cyanobacteria Leptolyngbya into Arabidopsis and Panicum roots, and Streptomyces into cassava roots. Some abundant microbes such as Sakaguchia in rice shoots or Vermispora in Arabidopsis roots appeared in no other samples, suggesting that they were infrequent, stochastically deposited propagules from either soil or seed (impossible to know based on the available data). Future experiments with culturing and cross-inoculation of these microbes between plants may help us better understand host preferences and their role in plant productivity, perhaps leading to their use in crop microbiome engineering and enhancement of agricultural production.

Effects of Inbreeding on Microbial Community Diversity ofZea mays

“…First, we showed that root communities were very similar to the rhizosphere soil, while only a fraction of these bacteria can be found in stalk tissue (Figure 1). This may be due to a combination of strong filters as bacteria travel up the plant [73, 74], or a larger effect of seed-transmitted microbes in the stalks compared to the roots [73]. Stalk samples had fewer ASVs overall and lower reads, and had a much smaller common microbiome when compared to root and rhizosphere (Figure 2).…”

Effects of Inbreeding on Microbial Community Diversity of Zea mays

“…First, we showed that root communities were very similar to the rhizosphere soil, while only a fraction of these bacteria can be found in stalk tissue (Figure 1). This may be due to a combination of strong filters as bacteria travel up the plant [78,79] or a larger effect of seed-transmitted microbes in the stalks compared to the roots [78]. It has been shown that endophytes can travel and persist in different tissues in maize [35].…”

Unlocking the potential of bacterial endophytes from medicinal plants for drug discovery

“…It is widely acknowledged that plants acquire most of their endophytes from the rhizosphere (Compant et al., 2021), although some studies have also demonstrated the direct transfer of endophytes via seeds (Johnston‐Monje et al., 2022). Plant roots extrude into soil substances such as cellulose, organic, amino and fatty acids, phenolics, plant growth hormones, nucleotides, sugars, sterols and vitamins that attract microorganisms and can be used by them as nutritional sources, (Sasse et al., 2018).…”