Comparative Analyses of Phyllosphere Bacterial Communities and Metabolomes in Newly Developed Needles of Cunninghamia lanceolata (Lamb.) Hook. at Four Stages of Stand Growth

Abstract

Host-plant-associated bacteria affect the growth, vigor, and nutrient availability of the host plant. However, phyllosphere bacteria have received less research attention and their functions remain elusive, especially in forest ecosystems. In this study, we collected newly developed needles from sapling (age 5 years), juvenile (15 years), mature (25 years), and overmature (35 years) stands of Chinese fir [Cunninghamia lanceolata (Lamb.) Hook]. We analyzed changes in phyllosphere bacterial communities, their functional genes, and metabolic activity among different stand ages. The results showed that phyllosphere bacterial communities changed, both in relative abundance and in composition, with an increase in stand age. Community abundance predominantly changed in the orders Campylobacterales, Pseudonocardiales, Deinococcales, Gemmatimonadales, Betaproteobacteriales, Chthoniobacterales, and Propionibacteriales. Functional predictions indicated the genes of microbial communities for carbon metabolism, nitrogen metabolism, antibiotic biosynthesis, flavonoids biosynthesis, and steroid hormone biosynthesis varied; some bacteria were strongly correlated with some metabolites. A total of 112 differential metabolites, including lipids, benzenoids, and flavonoids, were identified. Trigonelline, proline, leucine, and phenylalanine concentrations increased with stand age. Flavonoids concentrations were higher in sapling stands than in other stands, but the transcript levels of genes associated with flavonoids biosynthesis in the newly developed needles of saplings were lower than those of other stands. The nutritional requirements and competition between individual trees at different growth stages shaped the phyllosphere bacterial community and host–bacteria interaction. Gene expression related to the secondary metabolism of shikimate, mevalonate, terpenoids, tocopherol, phenylpropanoids, phenols, alkaloids, carotenoids, betains, wax, and flavonoids pathways were clearly different in Chinese fir at different ages. This study provides an overview of phyllosphere bacteria, metabolism, and transcriptome in Chinese fir of different stand ages and highlights the value of an integrated approach to understand the molecular mechanisms associated with biosynthesis.

Sphingomonas sp. Hbc-6 alters physiological metabolism and recruits beneficial rhizosphere bacteria to improve plant growth and drought tolerance

“…An observation confirmed that Bacillus in tomato leaf microbiota caused systematic exudation of acylsugar secondary metabolites in tomatoes (Korenblum et al, 2020). Some bacterial communities in the leaf layer of Cunninghamia lanceolata were closely related to some types of leaf metabolites, such as alkaloids, aldehydes, vitamins, azoles, and phenols, as reported by Sun et al (2021). In this study, we found that Hbc-6 mediated the significant correlation between some beneficial bacteria and metabolites under both normal and drought stress conditions (Figure 6).…”

“…Recent studies have focused on the interaction between plant-related microorganisms and plant secondary metabolites ( Korenblum et al., 2020 ; Sun et al., 2021 ; Xia et al., 2021 ). An observation confirmed that Bacillus in tomato leaf microbiota caused systematic exudation of acylsugar secondary metabolites in tomatoes ( Korenblum et al., 2020 ).…”

Endomicrobiome of in vitro and natural plants deciphering the endophytes-associated secondary metabolite biosynthesis in Picrorhiza kurrooa , a Himalayan medicinal herb

“…The presence of gene clusters of secondary metabolites and type VI gene clusters in Duganella species, many of which have antifungal properties, and the production of violacein, a major antibiotic, has been also established in many studies ( 132 – 135 ). The association of endophytic Duganella with secondary metabolites such as alkaloids and others has previously been also observed in Chinese fir ( 136 ). Bradyrhizobium is an Alphaproteobacteria that can undergo nitrogen-fixation symbiosis in the roots of many crops ( 137 ) found to contain gene clusters responsible for the biosynthesis of terpenes ( 138 ), phenolic compounds such as coumestrol ( 139 ), and alkaloids such as monocrotaline ( 140 ), linking their role in the production of secondary metabolites usually produced by the host.…”