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Abstract The 3-hydroxypropionate/4-hydroxybutyrate (3HP/4HB) cycle from ammonia-oxidizing Thaumarchaeota is currently considered the most energy-efficient aerobic carbon fixation pathway. TheNitrosopumilus maritimus4-hydroxybutyryl-CoA synthetase (ADP-forming; Nmar_0206) represents one of several enzymes from this cycle that exhibit increased efficiency over crenarchaeal counterparts. This enzyme reduces energy requirements on the cell, reflecting thaumarchaeal success in adapting to low-nutrient environments. Here we show the structure of Nmar_0206 fromNitrosopumilus maritimusSCM1, which reveals a highly conserved interdomain linker loop between the CoA-binding and ATP-grasp domains. Phylogenetic analysis suggests the widespread prevalence of this loop and highlights both its underrepresentation within the PDB and structural importance within the (ATP-forming) acyl-CoA synthetase (ACD) superfamily. This linker is shown to have a possible influence on conserved interface interactions between domains, thereby influencing homodimer stability. These results provide a structural basis for the energy efficiency of this key enzyme in the modified 3HP/4HB cycle of Thaumarchaeota. 

Abstract The Order Pelagibacterales (SAR11) is the most abundant group of heterotrophic bacterioplankton in global oceans and comprises multiple subclades with unique spatiotemporal distributions. Subclade IIIa is the primary SAR11 group in brackish waters and shares a common ancestor with the dominant freshwater IIIb (LD12) subclade. Despite its dominance in brackish environments, subclade IIIa lacks systematic genomic or ecological studies. Here, we combine closed genomes from new IIIa isolates, new IIIa MAGS from San Francisco Bay (SFB), and 460 highly complete publicly available SAR11 genomes for the most comprehensive pangenomic study of subclade IIIa to date. Subclade IIIa represents a taxonomic family containing three genera (denoted as subgroups IIIa.1, IIIa.2, and IIIa.3) that had distinct ecological distributions related to salinity. The expansion of taxon selection within subclade IIIa also established previously noted metabolic differentiation in subclade IIIa compared to other SAR11 subclades such as glycine/serine prototrophy, mosaic glyoxylate shunt presence, and polyhydroxyalkanoate synthesis potential. Our analysis further shows metabolic flexibility among subgroups within IIIa. Additionally, we find that subclade IIIa.3 bridges the marine and freshwater clades based on its potential for compatible solute transport, iron utilization, and bicarbonate management potential. Pure culture experimentation validated differential salinity ranges in IIIa.1 and IIIa.3 and provided detailed IIIa cell size and volume data. This study is an important step forward for understanding the genomic, ecological, and physiological differentiation of subclade IIIa and the overall evolutionary history of SAR11. 

Beach aquifers, located in the subsurface of sandy beaches, are unique ecosystems with steep chemical and physical gradients resulting from the mixing of terrestrial fresh groundwater and saline groundwater from the sea. While work has rapidly progressed to understand the physics and chemistry in this environment, much less is known about the microorganisms present despite the fact that they are responsible for vital biogeochemical processes. This paper presents a review of the current state of knowledge of microbes within beach aquifers and the mechanisms that control the beach aquifer microbiome. We review literature describing the distribution and diversity of microorganisms in the freshwater-saltwater mixing zone of beach aquifers, and identify just 12 papers. We highlight knowledge gaps, as well as future research directions: The understanding of beach aquifer microorganisms is informed primarily by 16S ribosomal RNA gene sequences. Metagenomics and metatranscriptomics have not yet been applied but are promising approaches for elucidating key metabolic and ecological roles of microbes in this environment. Additionally, variability in field sampling and analytical methods restrict comparison of data across studies and geographic locations. Further, documented evidence on the migration of microbes within the beach aquifer is limited. Taking into account the physical transport of microbes through sand by flowing groundwater may be critical for understanding the structure and dynamics of microbial communities. Quantitative measurements of rates of elemental cycling in the context of microbial diversity need further investigation, in order to understand the roles of microbes in mediating biogeochemical fluxes from the beach aquifer to the coastal ocean. Lastly, understanding the current state of beach aquifers in regulating carbon stocks is critical to foster a better understanding of the contribution of the beach aquifer microbiome to global climate models.