Title: Ecophysiology and genomics of the brackish water adapted SAR11 subclade IIIa
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. more »« less
Getz, Eric W.; Lanclos, V. Celeste; Kojima, Conner Y.; Cheng, Chuankai; Henson, Michael W.; Schön, Max Emil; Ettema, Thijs J.; Faircloth, Brant C.; Thrash, J. Cameron
(, mSystems)
Makhalanyane, Thulani P.
(Ed.)
One goal of marine microbiologists is to uncover the roles various microorganisms are playing in biogeochemical cycles. Success in this endeavor relies on differentiating groups of microbes and circumscribing their relationships. An early-diverging group (subclade V) of the most abundant bacterioplankton, SAR11, has recently been proposed as a separate lineage that does not share a most recent common ancestor. But beyond phylogenetics, little has been done to evaluate how these organisms compare with SAR11. Our work leverages dozens of new genomes to demonstrate the similarities and differences between subclade V and SAR11. In our analysis, we also establish that subclade V is synonymous with a group of bacteria established from 16S rRNA gene sequences, AEGEAN-169. Subclade V/AEGEAN-169 has clear metabolic distinctions from SAR11 and their shared traits point to remarkable convergent evolution if they do not share a most recent common ancestor.
Savoie, Emily R.; Lanclos, V. Celeste; Henson, Michael W.; Cheng, Chuankai; Getz, Eric W.; Barnes, Shelby J.; LaRowe, Douglas E.; Rappé, Michael S.; Thrash, J. Cameron
(, mSystems)
Poretsky, Rachel
(Ed.)
ABSTRACT Among the thousands of species that comprise marine bacterioplankton communities, most remain functionally obscure. One key cosmopolitan group in this understudied majority is the OM252 clade of Gammaproteobacteria . Although frequently found in sequence data and even previously cultured, the diversity, metabolic potential, physiology, and distribution of this clade has not been thoroughly investigated. Here, we examined these features of OM252 bacterioplankton using a newly isolated strain and genomes from publicly available databases. We demonstrated that this group constitutes a globally distributed novel genus (“ Candidatus Halomarinus”), sister to Litoricola , comprising two subclades and multiple distinct species. OM252 organisms have small genomes (median, 2.21 Mbp) and are predicted obligate aerobes capable of alternating between chemoorganoheterotrophic and chemolithotrophic growth using reduced sulfur compounds as electron donors. Subclade I genomes encode genes for the Calvin-Benson-Bassham cycle for carbon fixation. One representative strain of subclade I, LSUCC0096, had extensive halotolerance and a mesophilic temperature range for growth, with a maximum rate of 0.36 doublings/h at 35°C. Cells were curved rod/spirillum-shaped, ∼1.5 by 0.2 μm. Growth yield on thiosulfate as the sole electron donor under autotrophic conditions was roughly one-third that of heterotrophic growth, even though calculations indicated similar Gibbs energies for both catabolisms. These phenotypic data show that some “ Ca. Halomarinus” organisms can switch between serving as carbon sources or sinks and indicate the likely anabolic cost of lithoautotrophic growth. Our results thus provide new hypotheses about the roles of these organisms in global biogeochemical cycling of carbon and sulfur. IMPORTANCE Marine microbial communities are teeming with understudied taxa due to the sheer numbers of species in any given sample of seawater. One group, the OM252 clade of Gammaproteobacteria , has been identified in gene surveys from myriad locations, and one isolated organism has even been genome sequenced (HIMB30). However, further study of these organisms has not occurred. Using another isolated representative (strain LSUCC0096) and publicly available genome sequences from metagenomic and single-cell genomic data sets, we examined the diversity within the OM252 clade and the distribution of these taxa in the world’s oceans, reconstructed the predicted metabolism of the group, and quantified growth dynamics in LSUCC0096. Our results generate new knowledge about the previously enigmatic OM252 clade and point toward the importance of facultative chemolithoautotrophy for supporting some clades of ostensibly “heterotrophic” taxa.
Lee, Michael D.; Ahlgren, Nathan A.; Kling, Joshua D.; Walworth, Nathan G.; Rocap, Gabrielle; Saito, Mak A.; Hutchins, David A.; Webb, Eric A.
(, Environmental Microbiology)
Summary Synechococcus, a genus of unicellular cyanobacteria found throughout the global surface ocean, is a large driver of Earth's carbon cycle. Developing a better understanding of its diversity and distributions is an ongoing effort in biological oceanography. Here, we introduce 12 new draft genomes of marineSynechococcusisolates spanning five clades and utilize ~100 environmental metagenomes largely sourced from the TARA Oceans project to assess the global distributions of the genomic lineages they and other reference genomes represent. We show that five newly provided clade‐II isolates are by far the most representative of the recoveredin situpopulations (most ‘abundant’) and have biogeographic distributions distinct from previously available clade‐II references. Additionally, these isolates form a subclade possessing the smallest genomes yet identified of the genus (2.14 ± 0.05Mbps; mean ± 1SD) while concurrently hosting some of the highest GC contents (60.67 ± 0.16%). This is in direct opposition to the pattern inSynechococcus’s nearest relative,Prochlorococcus– wherein decreasing genome size has coincided with a strongdecreasein GC content – suggesting this new subclade ofSynechococcusappears to have convergently undergone genomic reduction relative to the rest of the genus, but along a fundamentally different evolutionary trajectory.
Abstract Understanding the ecological factors that shape geographic range limits and the evolutionary constraints that prevent populations from adaptively evolving beyond these limits is an unresolved question. Here, we investigated why the euryhaline fish,Poecila reticulata, is confined to freshwater within its native range, despite being tolerant of brackish water. We hypothesised that competitive interactions with a close relative,Poecilia picta, in brackish water preventsP.reticulatafrom colonising brackish water. Using a combination of field transplant, common garden breeding, and laboratory behaviour experiments, we find support for this hypothesis, asP.reticulataare behaviourally subordinate and have lower survival in brackish water withP.picta. We also found a negative genetic correlation betweenP.reticulatagrowth in brackish water versus freshwater in the presence ofP.picta, suggesting a genetically based trade‐off between salinity tolerance and competitive ability could constrain adaptive evolution at the range limit.
Abstract Coastal ecosystems are exposed to saltwater intrusion but differential effects on biogeochemical cycling are uncertain. We tested how elevated salinity and phosphorus (P) individually and interactively affect microbial activities and biogeochemical cycling in freshwater and brackish wetland soils. In experimental mesocosms, we added crossed gradients of elevated concentrations of soluble reactive P (SRP) (0, 20, 40, 60, 80 μg/L) and salinity (0, 4, 7, 12, 16 ppt) to freshwater and brackish peat soils (10, 14, 17, 22, 26 ppt) for 35 d. We quantified changes in water chemistry [dissolved organic carbon (DOC), ammonium (), nitrate + nitrite (N + N), SRP concentrations], soil microbial extracellular enzyme activities, respiration rates, microbial biomass C, and soil chemistry (%C, %N, %P, C:N, C:P, N:P). DOC, , and SRP increased in freshwater but decreased in brackish mesocosms with elevated salinity. DOC similarly decreased in brackish mesocosms with added P, and N + N decreased with elevated salinity in both freshwater and brackish mesocosms. In freshwater soils, water column P uptake occurred only in the absence of elevated salinity and when P was above 40 µg/L. Freshwater microbial EEAs, respiration rates, and microbial biomass C were consistently higher compared to those from brackish soils, and soil phosphatase activities and microbial respiration rates in freshwater soils decreased with elevated salinity. Elevated salinity increased arylsulfatase activities and microbial biomass C in brackish soils, and elevated P increased microbial respiration rates in brackish soils. Freshwater soil %C, %N, %P decreased and C:P and N:P increased with elevated salinity. Elevated P increased %C and C:N in freshwater soils and increased %P but decreased C:P and N:P in brackish soils. Freshwater soils released more C and nutrients than brackish soils when exposed to elevated salinity, and both soils were less responsive to elevated P than expected. Freshwater soils became more nutrient‐depleted with elevated salinity, whereas brackish soils were unaffected by salinity but increased P uptake. Microbial activities in freshwater soils were inhibited by elevated salinity and unaffected by added P, but brackish soil microbial activities slightly increased with elevated salinity and P.
Lanclos, V. Celeste, Rasmussen, Anna N., Kojima, Conner Y., Cheng, Chuankai, Henson, Michael W., Faircloth, Brant C., Francis, Christopher A., and Thrash, J. Cameron. Ecophysiology and genomics of the brackish water adapted SAR11 subclade IIIa. The ISME Journal 17.4 Web. doi:10.1038/s41396-023-01376-2.
Lanclos, V. Celeste, Rasmussen, Anna N., Kojima, Conner Y., Cheng, Chuankai, Henson, Michael W., Faircloth, Brant C., Francis, Christopher A., & Thrash, J. Cameron. Ecophysiology and genomics of the brackish water adapted SAR11 subclade IIIa. The ISME Journal, 17 (4). https://doi.org/10.1038/s41396-023-01376-2
Lanclos, V. Celeste, Rasmussen, Anna N., Kojima, Conner Y., Cheng, Chuankai, Henson, Michael W., Faircloth, Brant C., Francis, Christopher A., and Thrash, J. Cameron.
"Ecophysiology and genomics of the brackish water adapted SAR11 subclade IIIa". The ISME Journal 17 (4). Country unknown/Code not available: Oxford University Press. https://doi.org/10.1038/s41396-023-01376-2.https://par.nsf.gov/biblio/10395257.
@article{osti_10395257,
place = {Country unknown/Code not available},
title = {Ecophysiology and genomics of the brackish water adapted SAR11 subclade IIIa},
url = {https://par.nsf.gov/biblio/10395257},
DOI = {10.1038/s41396-023-01376-2},
abstractNote = {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.},
journal = {The ISME Journal},
volume = {17},
number = {4},
publisher = {Oxford University Press},
author = {Lanclos, V. Celeste and Rasmussen, Anna N. and Kojima, Conner Y. and Cheng, Chuankai and Henson, Michael W. and Faircloth, Brant C. and Francis, Christopher A. and Thrash, J. Cameron},
}
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