Large-scale phylogenomics of aquatic bacteria reveal molecular mechanisms for adaptation to salinity

Abstract

The crossing of environmental barriers poses major adaptive challenges. Rareness of freshwater-marine transitions separates the bacterial communities, but how these are related to brackish counterparts remains elusive, as do the molecular adaptations facilitating cross-biome transitions. We conducted large-scale phylogenomic analysis of freshwater, brackish, and marine quality-filtered metagenome-assembled genomes (11,248). Average nucleotide identity analyses showed that bacterial species rarely existed in multiple biomes. In contrast, distinct brackish basins cohosted numerous species, but their intraspecific population structures displayed clear signs of geographic separation. We further identified the most recent cross-biome transitions, which were rare, ancient, and most commonly directed toward the brackish biome. Transitions were accompanied by systematic changes in amino acid composition and isoelectric point distributions of inferred proteomes, which evolved over millions of years, as well as convergent gains or losses of specific gene functions. Therefore, adaptive challenges entailing proteome reorganization and specific changes in gene content constrains the cross-biome transitions, resulting in species-level separation between aquatic biomes.

A global atlas of subsurface microbiomes reveals phylogenetic novelty, large scale biodiversity gradients, and a marine-terrestrial divide

“…The taxonomic differentiation between marine and terrestrial microbial communities mirrors the differences between animal communities in these biomes ( 98 ) and is likely caused by the very different chemical and physical properties that shape these environments ( 99 ). The environmental drivers responsible for the gradients, continua, and divides remain undefined but they likely include factors such as salinity ( 100 , 101 ), energy availability ( 57 ), geological activity ( 102 , 103 ), hydrologic conditions and recharge rates ( 104 , 105 ), and constrictions of void space within which microbial cells might exist ( 94 ). Improvements in global scale modeling and increasing availability of data can provide the tools to describe the surface and subsurface on large scales, refine our insights into microbial provinces in the subsurface ( 106 ), and potentially define regions of similar subsurface biogeochemical regimes analogous to Longhurst provinces for the surface ocean ( 107 ).…”

Human‐induced salinity changes impact marine organisms and ecosystems

“…The CMIP6 Earth Systems Models (ESMs) that provide salinity and runoff change fields are detailed in the Supplementary Material & Methods (Tables S2-S4). Salinity is a major physicochemical factor determining bacterial community composition, and salinity differences pose a particularly strong barrier for microorganismic metabolism to overcome (Jurdzinski et al, 2023). Salinity drives soil and water microbiome global composition for both, prokaryotic and eukaryotic taxa (Herlemann et al, 2011;Lozupone & Knight, 2007;Shearer et al, 2007;Telesh et al, 2013).…”

Microbial ecology of coastal northern Gulf of Mexico waters

“…Salinity is known to be a major factor influencing microbial community structure and metabolic capacity (Lozupone and Knight 2007; Logares et al 2009; Walsh et al 2013; Dupont et al 2014). Regulatory, functional, and metabolic differences between closely related microbial taxa underpin preferences for different salinity regimes (Logares et al 2010; Salcher et al 2011; Dupont et al 2014; Henson et al 2018b; Cabello-Yeves et al 2022; Jurdzinski et al 2023). These important differences can prevent microorganisms from circumventing the marine-freshwater threshold, resulting in infrequent transitions between these environments within taxonomic clades (Logares et al 2009, 2010; Dupont et al 2014; Henson et al 2018b; Cabello-Yeves et al 2022; Lanclos et al 2023) and lower species diversity in intermediate salinities (Olli et al 2019), as first hypothesized in the Remane curve (Remane 1934).…”

“…Under future climate scenarios, estuaries are expected to be influenced by elevated land loss, as well as changes to salinity, pH, temperature, and other factors (Nicholls et al 2007; Elliott et al 2019; Reed et al 2020; Jurdzinski et al 2023), which could fundamentally alter the microbial community composition and ultimately the processing of carbon and other nutrients (Dupont et al 2014). Previous work has sought to investigate if brackish environments host autochthonous microbial communities uniquely adapted to these fluctuating ecosystems.…”