Genomic, metabolic and phenotypic variability shapes ecological differentiation and intraspecies interactions of Alteromonas macleodii

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.

Microbial Diversity of Co-occurring Heterotrophs in Cultures of Marine Picocyanobacteria

“…In addition to , which can outnumber cells by a factor of 10 or more, and marine heterotrophs like Alteromonas are capable of growing on these vesicles as a sole source of carbon (Biller, Schubotz, et al, 2014). Recent work also suggests that Alteromonas isolates derived from cultures of Prochlorococcus carry genes for the degradation of aromatic compounds produced by the cyanobacterium (Koch et al, 2020), which may provide a selective advantage. Additionally, metagenomics on a Synechococcus-associated culture revealed high abundance of TonB-dependent transporters in Muricauda, potentially involved in lipid uptake, and proteins involved in the export of lipids in the proteome of the Synechococcus host (Zheng et al, 2020).…”

Microbial Diversity of Co-occurring Heterotrophs in Cultures of Marine Picocyanobacteria

“…For instance, the most ubiquitous genus (present in over 60% of both culture types) is Marinobacter ( Figure 3C), which is well-known to be associated with picocyanobacteria in culture (Morris et al, 2008). In addition to Marinobacter, other genera present in at least 15% of cultures including Thalassospira, Methylophaga, Alteromonas, Alcanivorax, Maricaulis, Muricauda, and Hyphomonas (but not Shimia) have been associated with metabolism of hydrocarbons or C1 compounds derived from lipid catabolism (Coulon et al, 2007;Dong et al, 2018;Hara et al, 2003;Kappell et al, 2014;Koch et al, 2020;Kostka et al, 2011;Lea-Smith et al, 2015;Liu et al, 2007;López-Pérez et al, 2012;Neufeld et al, 2007;Vila et al, 2010;Yakimov et al, 2007;Zhao et al, 2010), suggesting that hydrocarbon metabolism might play an important role in their growth in these cultures. Indeed, previous work showed an upregulation of genes for fatty acid metabolism including lipid betaoxidation in co-culture of Alteromonas macleodii with Prochlorococcus (Biller et al, 2016).…”

“…Prochlorococcus secretes vesicles (potentially a source of lipids) in culture and in the wild (Biller et al, 2017;Biller, Schubotz, et al, 2014), which can outnumber cells by a factor of 10 or more, and marine heterotrophs like Alteromonas are capable of growing on these vesicles as a sole source of carbon (Biller, Schubotz, et al, 2014). Recent work also suggests that Alteromonas isolates derived from cultures of Prochlorococcus carry genes for the degradation of aromatic compounds produced by the cyanobacterium (Koch et al, 2020), which may provide a selective advantage. Additionally, metagenomics on a Synechococcusassociated culture revealed high abundance of TonB-dependent transporters in Muricauda, potentially involved in lipid uptake, and proteins involved in the export of lipids in the proteome of the Synechococcus host (Zheng et al, 2020).…”

Microbial Diversity of Co-occurring Heterotrophs in Cultures of Marine Picocyanobacteria

“…For instance, the most ubiquitous genus (present in over 60% of both culture types) is Marinobacter ( Figure 3C), which is wellknown to be associated with picocyanobacteria in culture (Morris et al, 2008). In addition to Marinobacter, other genera present in at least 15% of cultures including Thalassospira, Methylophaga, Alteromonas, Alcanivorax, Maricaulis, Muricauda, and Hyphomonas (but not Shimia) have been associated with metabolism of hydrocarbons or C1 compounds derived from lipid catabolism (Coulon et al, 2007;Dong et al, 2018;Hara et al, 2003;Kappell et al, 2014;Koch et al, 2020;Kostka et al, 2011;Lea-Smith et al, 2015;Liu et al, 2007;López-Pérez et al, 2012;Neufeld et al, 2007;Vila et al, 2010;Yakimov et al, 2007;Zhao et al, 2010), suggesting that hydrocarbon metabolism might play an important role in their growth in these cultures. Indeed, previous work showed an upregulation of genes for fatty acid metabolism including lipid beta-oxidation in co-culture of Alteromonas macleodii with Prochlorococcus (Biller et al, 2016).…”

“…Prochlorococcus secretes vesicles (potentially a source of lipids) in culture and in the wild (Biller et al, 2017;Biller, Schubotz, et al, 2014), which can outnumber cells by a factor of 10 or more, and marine heterotrophs like Alteromonas are capable of growing on these vesicles as a sole source of carbon (Biller, Schubotz, et al, 2014). Recent work also suggests that Alteromonas isolates derived from cultures of Prochlorococcus carry genes for the degradation of aromatic compounds produced by the cyanobacterium (Koch et al, 2020), which may provide a selective advantage. Additionally, metagenomics on a Synechococcus-associated culture revealed high abundance of TonB-dependent transporters in Muricauda, potentially involved in lipid uptake, and proteins involved in the export of lipids in the proteome of the Synechococcus host (Zheng et al, 2020).…”