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1. Metabolite diversity among representatives of divergent Prochlorococcus ecotypes

   https://doi.org/10.1128/msystems.01261-22  

   Kujawinski, Elizabeth B; Braakman, Rogier; Longnecker, Krista; Becker, Jamie W; Chisholm, Sallie W; Dooley, Keven; Kido_Soule, Melissa C; Swarr, Gretchen J; Halloran, Kathryn (October 2023, mSystems)

   Gilbert, Jack A (Ed.)

   ABSTRACT The euphotic zone of the surface ocean contains distinct physical-chemical regimes that vary in light and nutrient concentrations as an inverse function of depth. The most numerous phytoplankter of the mid- and low-latitude ocean is the picocyanobacteriumProchlorococcus, which consists of ecologically distinct subpopulations (i.e., “ecotypes”). Ecotypes have different temperature, light, and nutrient optima and display distinct relative abundances along gradients of these niche dimensions. As a primary producer,Prochlorococcusfixes and releases organic carbon to neighboring microbes as part of the microbial loop. However, little is known about the specific moleculesProchlorococcusaccumulates and releases or how these processes vary among its ecotypes. Here, we characterize the metabolite diversity ofProchlorococcusby profiling three ecologically distinct cultured strains: MIT9301, representing a high-light-adapted ecotype dominating shallow tropical and sub-tropical waters; MIT0801, representing a low-light-adapted ecotype found throughout the euphotic zone; and MIT9313, representing a low-light-adapted ecotype relatively most abundant at the base of the euphotic zone. In both intracellular and extracellular metabolite profiles, we observe striking differences across strains in the accumulation and release of molecules, such as the DNA methylating agent S-adenosyl-methionine (intracellular) and the branched-chain amino acids (intracellular) and their precursors (extracellular). While some differences reflect variable genome content across the strains, others likely reflect variable regulation of conserved pathways. In the extracellular profiles, we identify molecules such as pantothenic acid and aromatic amino acids that may serve as currencies inProchlorococcus’ interactions with neighboring microbes and, therefore, merit further investigation. IMPORTANCEApproximately half of the annual carbon fixation on Earth occurs in the surface ocean through the photosynthetic activities of phytoplankton such as the ubiquitous picocyanobacteriumProchlorococcus. Ecologically distinct subpopulations (or ecotypes) ofProchlorococcusare central conduits of organic substrates into the ocean microbiome, thus playing important roles in surface ocean production. We measured the chemical profile of three cultured ecotype strains, observing striking differences among them that have implications for the likely chemical impact ofProchlorococcussubpopulations on their surroundings in the wild. Subpopulations differ in abundance along gradients of temperature, light, and nutrient concentrations, suggesting that these chemical differences could affect carbon cycling in different ocean strata and should be considered in models ofProchlorococcusphysiology and marine carbon dynamics. 

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2. Comparing Prochlorococcus temperature niches in the lab and across ocean basins

   https://doi.org/10.1002/lno.11777  

   Smith, Alaina N.; Hennon, Gwenn M. M.; Zinser, Erik R.; Calfee, Benjamin C.; Chandler, Jeremy W.; Barton, Andrew D. (May 2021, Limnology and Oceanography)

   Abstract Niche theory suggests that the realized niche occupied by an organism in the field is a subset of the fundamental niche space of the organism, absent additional biotic and abiotic factors. Though often assumed, this discrepancy is rarely tested for specific organisms, and could act as a source of error in model predictions of biogeographical shifts resulting from temperature change which assume niche theory constraints. Here, we quantify the difference between fundamental and realized temperature niches for four dominant ecotypes ofProchlorococcus, including eMED4, eMIT9312, eMIT9313, and eNATL2A, and ask whether the realized temperature niches of each ecotype vary across ocean basins. The realized niches for the four ecotypes are, on average, 3.84°C ± 1.18°C colder (mean ± SD across all ocean basins and ecotypes) and 2.15°C ± 1.89°C wider than the lab‐measured fundamental niches. When divided into four ocean regions—North Atlantic, South Atlantic, North Pacific, and South Pacific—we find that the realized temperature niche optimum for a given ecotype compared to the fundamental temperature niche optimum differs across regions by as much as 7.93°C, while the niche width can differ by up to 9.48°C. Colder and wider realized niches may be a result of the metabolic risk associated with living in variable environments when the mean temperature is too close to the optimal temperature for growth or due to physical processes such as dispersal. The strong differences in temperature niches across ocean basins suggest that unresolved genetic diversity within ecotypes, local adaptation, and variable interactive ecological and environmental factors are likely to be important in shapingProchlorococcusrealized temperature niches. 

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3. Global scale phylogeography of functional traits and microdiversity in Prochlorococcus

   https://doi.org/10.1038/s41396-023-01469-y  

   Ustick, Lucas J.; Larkin, Alyse A.; Martiny, Adam C. (July 2023, The ISME Journal)

   Abstract Prochlorococcus is the most numerically abundant photosynthetic organism in the surface ocean. The Prochlorococcus high-light and warm-water adapted ecotype (HLII) is comprised of extensive microdiversity, but specific functional differences between microdiverse sub-clades remain elusive. Here we characterized both functional and phylogenetic diversity within the HLII ecotype using Bio-GO-SHIP metagenomes. We found widespread variation in gene frequency connected to local environmental conditions. Metagenome-assembled marker genes and genomes revealed a globally distributed novel HLII haplotype defined by adaptation to chronically low P conditions (HLII-P). Environmental correlation analysis revealed different factors were driving gene abundances verses phylogenetic differences. An analysis of cultured HLII genomes and metagenome-assembled genomes revealed a subclade within HLII, which corresponded to the novel HLII-P haplotype. This work represents the first global assessment of the HLII ecotype’s phylogeography and corresponding functional differences. These findings together expand our understanding of how microdiversity structures functional differences and reveals the importance of nutrients as drivers of microdiversity in Prochlorococcus. 

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4. Home-field advantage affects the local adaptive interaction between Andropogon gerardii ecotypes and root-associated bacterial communities

   https://doi.org/10.1128/spectrum.00208-23  

   Kazarina, Anna; Sarkar, Soumyadev; Thapa, Shiva; Heeren, Leah; Kamke, Abgail; Ward, Kaitlyn; Hartung, Eli; Ran, Qinghong; Galliart, Matthew; Jumpponen, Ari; et al (October 2023, Microbiology Spectrum)

   Arias, Renee S. (Ed.)

   ABSTRACT Due to climate change, drought frequencies and severities are predicted to increase across the United States. Plant responses and adaptation to stresses depend on plant genetic and environmental factors. Understanding the effect of those factors on plant performance is required to predict species’ responses to environmental change. We used reciprocal gardens planted with distinct regional ecotypes of the perennial grassAndropogon gerardiiadapted to dry, mesic, and wet environments to characterize their rhizosphere communities using 16S rRNA metabarcode sequencing. Even though the local microbial pool was the main driver of these rhizosphere communities, the significant plant ecotypic effect highlighted active microbial recruitment in the rhizosphere, driven by ecotype or plant genetic background. Our data also suggest that ecotypes planted at their homesites were more successful in recruiting rhizosphere community members that were unique to the location. The link between the plants’ homesite and the specific local microbes supported the “home field advantage” hypothesis. The unique homesite microbes may represent microbial specialists that are linked to plant stress responses. Furthermore, our data support ecotypic variation in the recruitment of congeneric but distinct bacterial variants, highlighting the nuanced plant ecotype effects on rhizosphere microbiome recruitment. These results improve our understanding of the complex plant host–soil microbe interactions and should facilitate further studies focused on exploring the functional potential of recruited microbes. Our study has the potential to aid in predicting grassland ecosystem responses to climate change and impact restoration management practices to promote grassland sustainability. IMPORTANCEIn this study, we used reciprocal gardens located across a steep precipitation gradient to characterize rhizosphere communities of distinct dry, mesic, and wet regional ecotypes of the perennial grassAndropogon gerardii. We used 16S rRNA amplicon sequencing and focused oligotyping analysis and showed that even though location was the main driver of the microbial communities, ecotypes could potentially recruit distinct bacterial populations. We showed that differentA. gerardiiecotypes were more successful in overall community recruitment and recruitment of microbes unique to the “home” environment, when growing at their “home site.” We found evidence for “home-field advantage” interactions between the host and host–root-associated bacterial communities, and the capability of ecotypes to recruit specialized microbes that were potentially linked to plant stress responses. Our study aids in a better understanding of the factors that affect plant adaptation, improve management strategies, and predict grassland function under the changing climate. 

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5. Ocean exposure and latitude drive multiple clines within the coastal perennial ecotype of the yellow monkeyflower, Mimulus guttatus

   https://doi.org/10.1002/ajb2.16402  

   Zambiasi, Thomas; Lowry, David B (September 2024, American Journal of Botany)

   Abstract PremiseA key goal of evolutionary biologists is to understand how and why genetic variation is partitioned within species. In the yellow monkeyflower,Mimulus guttatus(syn.Erythranthe guttata), coastal perennial populations constitute a single genetically and morphologically differentiated ecotype compared to inlandM. guttatuspopulations. While the coastal ecotype's distinctiveness has now been well documented, there is also environmental variation across the ecotype's range that could drive more continuous differentiation among its component populations. MethodsBased on previous observations of a potential cline within this ecotype, we quantified plant height, among other traits, across coastal perennial accessions from 74 populations in a greenhouse common garden experiment. To evaluate potential drivers of the relationship between trait variation and latitude, we regressed height against multiple climatic factors, including temperature, precipitation, and coastal wind speeds. We also accounted for exposure to the open ocean in all analyses. ResultsMultiple traits were correlated with latitude of origin, but none more than plant height. Height was negatively correlated with latitude, and plants directly exposed to the open ocean were shorter than those protected from coastal winds. Further analyses revealed that height was correlated with climatic factors (precipitation, temperature, and wind speeds) that were autocorrelated with latitude. We hypothesize that one or more of these climatic factors drove the evolution of latitudinal clinal variation within the coastal ecotype. ConclusionsOverall, our study illustrates the complexity of how the distribution of environmental variation can simultaneously drive the evolution of both distinct ecotypesandcontinuous clines within those ecotypes. 

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