Favorable habitats of endangered halophytes harbor unique soil properties and bacterial communities, with a dominant root-associated genus promoting host plant growth

Abstract

Understanding how edaphic factors and root-associated bacterial communities interact to shape plant growth is essential for effective conservation of halophytic species in coastal ecosystems. We investigated relationships among bulk soil, rhizosphere, and root bacterial microbiota; soil physicochemical properties; and Salicornia europaea growth spanning three distinct areas (Lakeside Park, Ubaranai and Misaki) within a brackish lake in Japan. Among the three study areas, S. europaea individuals from Lakeside Park exhibited the highest mean values for shoot length, fresh weight, dry weight, and number of primary branches, which were 1.9-, 11.2-, 12.1-, and 7.2-fold higher than those at Misaki in 2021, and 1.8-, 4.7-, 6.7-, and 4.7-fold higher than those at Misaki in 2022. Bacterial diversity and community composition associated with S. europaea varied in response to differences in plant growth and edaphic conditions. Soil texture, electrical conductivity, pH, total organic carbon, total nitrogen, C/N ratio, and water-soluble Ca 2+ were identified as key factors underlying microbial community structures. Based on heatmap and LEfse analyses, six bacterial genera, Bacteroidetes BD2-2, Candidatus Thiobios , SEEP-SRB1, Calditrichaceae , Bacteroidetes VC2.1 Bac22, and Luteibacter , were significantly enriched in areas where S. europaea exhibited vigorous growth. Among these, Luteibacter was consistently identified as the unique and dominant genus in root samples from the most favorable habitats. Inoculation experiments further demonstrated that L. aegosomatis and L. jiangsuensis significantly enhanced S. europaea growth, with shoot length, fresh weight, and dry weight being 1.4- and 1.2-, 2.1- and 1.6-, and 1.9- and 1.5-fold higher, respectively, than those of non-inoculated controls. These findings highlight that soil physicochemical conditions modulate root-associated bacterial assemblages and that a unique and dominant root-associated genus in favorable habitats may include strains capable of promoting S. europaea growth. Our results provide new ecological insights into plant–microbe–soil interactions and offer a promising framework for in situ conservation and restoration of rare halophytic species in brackish ecosystems.