Ecotypic differentiation within abundant Magnimaribacterales marine bacteria

Abstract

The bacterial clade SAR86, recently reclassified as the order Magnimaribacterales, is one of the most abundant and globally distributed groups of heterotrophic bacteria in surface ocean waters. Despite being discovered thirty years ago, our understanding of its ecology and evolution still has significant gaps. This dissertation addresses these gaps through a combination of comparative genomics and metagenomic analyses drawn from a range of marine environments. In Chapter 2, a phylogenomic survey of over 700 genomes— including those from major global ocean surveys and the first fully sequenced cultured representative— reveals that Magnimaribacterales comprises four distinct families, each containing multiple clades with different biogeographical distributions. Although the capacity for fatty acid degradation via β-oxidation is broadly conserved, certain clades exhibit additional metabolic specializations such as α-oxidation and pathways for degrading complex, steroid-like polycyclic compounds. These findings indicate that a few dominant clades account for much of the group’s global abundance, while many others are more spatially restricted. Chapter 3 focuses on the ecological differentiation of Magnimaribacterales within Kāneʻohe Bay, Hawaiʻi, a coastal environment characterized by strong spatial gradients. Here, habitat-specific genotypes were identified, with niche specialization linked to differences in sugar metabolism and membrane biosynthesis, suggesting fine-scale adaptation to distinct inshore and offshore conditions. In Chapter 4, the vertical distribution of Magnimaribacterales is examined across the stratified water column of the North Pacific Ocean. Certain lineages are confined to surface waters, while others are enriched at depth and possess genes associated with the breakdown of more chemically recalcitrant organic compounds, highlighting functional adaptation to carbon-limited environments. Taken together, these findings demonstrate that Magnimaribacterales is a phylogenetically diverse and functionally versatile lineage that has undergone extensive ecological diversification, enabling it to thrive across a various marine environments and help sto start to explain its ubiquitous presence in the global oceans.