Abstract

Ecological differentiation between strains of bacterial species is shaped by genomic and metabolic variability. However, connecting genotypes to ecological niches remains a major challenge. Here, we linked bacterial geno- and phenotypes by contextualizing pangenomic, exometabolomic and physiological evidence in twelve strains of the marine bacterium Alteromonas macleodii, illuminating adaptive strategies of carbon metabolism, microbial interactions, cellular communication and iron acquisition. In A. macleodii strain MIT1002, secretion of amino acids and the unique capacity for phenol degradation may promote associations with Prochlorococcus cyanobacteria. Strain 83-1 and three novel Pacific isolates, featuring clonal genomes despite originating from distant locations, have profound abilities for algal polysaccharide utilization but without detrimental implications for Ecklonia macroalgae. Degradation of toluene and xylene, mediated via a plasmid syntenic to terrestrial Pseudomonas, was unique to strain EZ55. Benzoate degradation by strain EC673 related to a chromosomal gene cluster shared with the plasmid of A. mediterranea EC615, underlining that mobile genetic elements drive adaptations. Furthermore, we revealed strain-specific production of siderophores and homoserine lactones, with implications for nutrient acquisition and cellular communication. Phenotypic variability corresponded to different competitiveness in co-culture and geographic distribution, indicating linkages between intraspecific diversity, microbial interactions and biogeography. The finding of “ecological microdiversity” helps understanding the widespread occurrence of A. macleodii and contributes to the interpretation of bacterial niche specialization, population ecology and biogeochemical roles.

Highlights

  • Metabolic variability is a major driver of ecological differentiation within bacterial taxa, shaping adaptive strategies and the niche space of related strains[1]

  • This variable repertoire is often encoded in genomic islands, hotspots of genetic exchange[5] known to influence niche specialization in cyanobacteria, actinobacteria and roseobacters[6,7,8]

  • The shown intraspecific diversity in adaptive strategies helps understanding the widespread occurrence of A. macleodii in the oceans, with broader implications for bacterial population ecology and niche specialization

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Summary

Introduction

Metabolic variability is a major driver of ecological differentiation within bacterial taxa, shaping adaptive strategies and the niche space of related strains[1]. The occupation of different niches[24], varied interactions with other organisms[25,26,27] and utilization of diverse substrates[28,29] suggests the existence of functionally distinct entities within the A. macleodii species boundary, despite being >99% identical on 16S rRNA gene level This notion is supported by the diverse flexible genome and a high degree of genetic exchange between A. macleodii and the “sister species” A. mediterranea[13,30]. A. mediterranea strains differ in motility and glucose utilization, potentially influencing patterns of co-occurrence or mutual exclusion[35] Despite these ecological implications of genome plasticity, phenotypic and genomic variability have not been comprehensively linked in Alteromonas to date, largely because few putative traits have been experimentally verified. The shown intraspecific diversity in adaptive strategies helps understanding the widespread occurrence of A. macleodii in the oceans, with broader implications for bacterial population ecology and niche specialization

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