AUTHOR=Mondal Sumana , Biswas Biswajit , Chowdhury Rajojit , Sengupta Rudranil , Mandal Anup , Kotal Hemendra Nath , Giri Chayan Kumar , Ghosh Anjali , Saha Subhajit , Begam Mst Momtaj , Mukherjee Chandan , Das Ipsita , Basak Sandip Kumar , Mitra Ghosh Mahashweta , Ray Krishna 

TITLE=Estuarine mangrove niches select cultivable heterotrophic diazotrophs with diverse metabolic potentials—a prospective cross-dialog for functional diazotrophy

JOURNAL=Frontiers in Microbiology

VOLUME=Volume 15 - 2024

YEAR=2024

URL=https://www.frontiersin.org/journals/microbiology/articles/10.3389/fmicb.2024.1324188

DOI=10.3389/fmicb.2024.1324188

ISSN=1664-302X

ABSTRACT=Biological nitrogen fixation (BNF), an unparalleled metabolic novelty among living microorganisms on earth, globally contributes ~88-101 Tg N year -1 to natural ecosystems, ~56% sourced from symbiotic BNF while ~22-45% derived from free-living nitrogen fixers (FLNF). The success of symbiotic BNF is largely dependent on its interaction with hostplant, however ubiquitous environmental heterotrophic FLNFs face many limitations in their immediate ecological niches to sustain unhindered BNF. The autotrophic FLNFs like cyanobacteria and oceanic heterotrophic diazotrophs have been well studied about their contrivances acclimated/adapted by these organisms to outwit the environmental constraints for functional diazotrophs. However, FLNF heterotrophs face more adversity in executing BNF under stressful estuarine/marine/aquatic habitats. In this study a large-scale cultivationdependent investigation was accomplished with 190 NCBI accessioned and 45 nonaccessioned heterotrophic FLNF cultivable bacterial isolates (total 235) from halophilic estuarine intertidal mangrove niches of Indian Sundarbans, a Ramsar site and UNESCO proclaimed World Heritage Site. Assuming ~1% culturability of the microbial community, the respective niches were also studied for representing actual bacterial diversity via cultivation-independent next-generation sequencing of V3-V4 rRNA regions. Both the studies revealed a higher abundance of culturable Gammaproteobacteria followed by Firmicutes, the majority of 235 FLNFs studied belonging to these two classes. The FLNFs displayed comparable selection potential in media for free nitrogen fixers and iron-oxidizing bacteria, linking diazotrophy with iron oxidation, siderophore production, phosphorus solubilization, phosphorus uptake and accumulation as well as denitrification. This observation validated the hypothesis that under extreme estuarine mangrove niches, diazotrophs are naturally selected as a specialized multidimensional entity, to expedite BNF and survive. Earlier metagenome data from mangrove niches demonstrated a microbial metabolic coupling among C, N, P, S, and Fe cycling in mangrove sediments, as an adaptive trait, evident with the co-abundant respective functional genes, which corroborates our findings in cultivation mode for multiple interrelated metabolic potential facilitating BNF in a challenging intertidal mangrove environment.