Metagenomic assembled genomes indicated the potential application of hypersaline microbiome for plant growth promotion and stress alleviation in salinized soils

Abstract

Climate change is causing unpredictable seasonal variations globally. Due to the continuously increasing earth's surface temperature, the rate of water evaporation is enhanced, conceiving a problem of soil salinization, especially in arid and semi-arid regions. The accumulation of salt degrades soil quality, impairs plant growth, and reduces agricultural yields. Salt-tolerant, plant-growth-promoting microorganisms may offer a solution, enhancing crop productivity and soil fertility in salinized areas. In the current study, genome-resolved metagenomic analysis has been performed to investigate the salt-tolerating and plant growth-promoting potential of two hypersaline ecosystems, Sambhar Lake and Drang Mine. The samples were co-assembled independently by Megahit, MetaSpades, and IDBA-UD tools. A total of 67 metagenomic assembled genomes (MAGs) were reconstructed following the binning process, including 15 from Megahit, 26 from MetaSpades, and 26 from IDBA_UD assembly tools. As compared to other assemblers, the MAGs obtained by MetaSpades were of superior quality, with a completeness range of 12.95%-96.56% and a contamination range of 0%-8.65%. The medium and high-quality MAGs from MetaSpades, upon functional annotation, revealed properties such as salt tolerance (91.3%), heavy metal tolerance (95.6%), exopolysaccharide (95.6%), and antioxidant (60.86%) biosynthesis. Several plant growth-promoting attributes, including phosphate solubilization and indole-3-acetic acid (IAA) production, were consistently identified across all obtained MAGs. Conversely, characteristics such as iron acquisition and potassium solubilization were observed in a substantial majority, specifically 91.3%, of the MAGs. The present study indicates that hypersaline microflora can be used as bio-fertilizing agents for agricultural practices in salinized areas by alleviating prevalent stresses.

Importance: The strategic implementation of metagenomic assembled genomes (MAGs) in exploring the properties and harnessing microorganisms from ecosystems like hypersaline niches has transformative potential in agriculture. This approach promises to redefine our comprehension of microbial diversity and its ecosystem roles. Recovery and decoding of MAGs unlock genetic resources, enabling the development of new solutions for agricultural challenges. Enhanced understanding of these microbial communities can lead to more efficient nutrient cycling, pest control, and soil health maintenance. Consequently, traditional agricultural practices can be improved, resulting in increased yields, reduced environmental impacts, and heightened sustainability. MAGs offer a promising avenue for sustainable agriculture, bridging the gap between cutting-edge genomics and practical field applications.

Keywords: heavy metal stress; hypersaline ecosystems; metagenomic assembled genomes; plant growth promotion; salinized soil; salt stress.

Fig 1

of the reconstructed MAGs. (A) Heatmap showing the different values of MAGs quality: completeness, contamination, genome size, and N50 values. (B) Phylogenetic visualization of recovered MAGs, where black-colored branches represent low-quality, pink-colored branches represent medium-quality, and blue-colored branches show high-quality MAGs.

Fig 2

Taxonomic classification and functional annotation of medium- and high-quality MAGs. The functional analysis revealed genetic evidence for salt tolerance, heavy metal tolerance, and plant growth-promoting potential of hypersaline microflora. The right side of the heatmap displays the hierarchical clustering of the MAGs based on the occurrence of the different genetic attributes.

Fig 3

Pan-genome and average nucleotide identity (ANI) visualization of MAGs with the genome of their respective genera. (A) Comparison of IDBA_017 and Metaspades_003 with the genomes of the genus Natronomonas. The MAGs IDBA_017 and Metaspades_003 showed ANI values of 97.62 and 97.6 for Natronomonas pharaonis, respectively. (B) Comparison of the MAG Metaspades_015 to the genomes of the genus Spiribacter. Metaspades_015 showed the ANI value of 95.01 with Spiribacter 2438. (C) Illustration of various salt tolerance, heavy metal stress tolerance, and plant growth-promoting genetic features of IDBA_017, Metaspades_003 (D), and Metaspades_015 (E).