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Martiny, A. C.

Publications and source records attributed to Martiny, A. C..

7 recordsLinked to original sources

Decadal signatures of seasonal and ENSO-driven selection in microbial populations in distant oceans

Despite the crucial role of the ocean microbiome for global ecosystem processes, its response to global change remains poorly understood. Global change will exert selection on microbial species through changes in the genetic composition of their populations, favouring strains that are better adapted to new conditions. Analyzing long-term genomic variation in microbial populations inhabiting climatically comparable but oceanographically distinct regions may provide insights into their responses to future environmental conditions. We analyzed coastal marine microbiomes from two distant long-term observatories with Mediterranean-type climates but contrasting oceanographic regimes: the Blanes Bay Microbial Observatory (BBMO; Northwestern Mediterranean Sea) and the Microbes in the Coastal Region of Orange County (MiCRO; California coast, Pacific Ocean). Sampling conducted at least monthly during 15 and 10 years, respectively, yielded 1,535 Metagenome-Assembled Genomes (MAGs) in BBMO and 1,068 MAGs plus 187 Single-Amplified Genomes (SAGs) in MiCRO. Among these, we found 250 genomes with intraspecific (>95% genome similarity) representatives occurring at both sites. In contrast, at the strain-level threshold ([≥]99% genome similarity), only 13 BBMO genomes matched 15 closely related representatives in MiCRO. As genome similarity increased, we observed a shift from cosmopolitan to more coastal distributions and a slight increase in genome size, pointing to niche adaptation. Across both time series, we observed widespread seasonal population structure, with most genomes (~70%) showing significant seasonal structuring of variant composition. Moreover, in MiCRO, ~76% of the tested genomes also showed El Nino Southern Oscillation (ENSO)-associated structure in variant composition beyond seasonal effects. Focusing on a Prochlorococcus genome with intraspecific representatives at both locations (>96% genome similarity) we further found recurrent seasonal mutations and non-synonymous to synonymous mutation ratios (pN/pS) from multiple genes, together with signatures of positive selection (higher pN/pS) coinciding with El Nino events in MiCRO. This suggests an imprint of ENSO in marine microbial populations. Thus, beyond seasonality, long-term climatic oscillations may shape microbial populations. This has implications for understanding how the ocean microbiome will respond to long-term environmental change and prolonged disturbances through population-level genomic variation.

microbiology↗

Enhanced carbon storage in dissolved organic matter in a future oligotrophic ocean

Marine dissolved organic carbon (DOC) is one of the oceans largest carbon reser-voirs, which persists for millennia and exceeds the carbon stored in terrestrial and marine biomass combined (Hansell et al, 2012; Dittmar et al, 2021; Moran et al, 2022). Yet its response to climate change remains uncertain, largely because the ecological mechanisms behind its microbial degradation are poorly understood (Wagner et al, 2020; Legendre et al, 2015; Lonborg et al, 2020). Here we show how observed global-scale distribution of DOC emerges from bottom-up ecological controls acting on microbial DOC consumers. We combined large-scale metagenomic data (Larkin et al, 2021) with incubation experiments (Hale et al, 2017) to map global patterns of nutrient limitation in heterotrophic microbial communities responsible for DOC uptake. We then integrated a new microbial-DOC component into an Earth system model, which successfully reproduced observed global distributions of nutrient stress and DOC concentrations. Linking carbon and nutrient cycles reveals quantitatively significant consequences for the future ocean. Under a highemission scenario (SSP5-8.5), the DOC pool is projected to increase by 18-44 gigatons by 2200. This increase, driven by intensified nutrient limitation in surface waters, contributes substantially to the biological carbon pump, accounting for about[~] 30% of the increase in deep-ocean carbon storage associated with particulate organic carbon export. Overall, our results indicate that the marine DOC reservoir is more dynamic than previously thought. Reduced DOC remineralisation in an increasingly oligotrophic ocean constitutes a quantitatively significant negative feedback on centennial timescales.

microbiology↗

Global Phylogeography and Microdiversity of the Marine Diazotrophic Cyanobacteria Trichodesmium and UCYN-A

Cyanobacterial diazotrophs, specifically the genera Trichodesmium and UCYN-A, play a pivotal role in marine nitrogen cycling through their capacity for nitrogen fixation. Despite their global distribution, the microdiversity and environmental drivers of these diazotrophs remain underexplored. This study provides a comprehensive analysis of the global diversity and distribution of Trichodesmium and UCYN-A using the nitrogenase gene (nifH) as a genetic marker. We sequenced 954 samples from the Pacific, Atlantic, and Indian Oceans as part of the Bio-GO-SHIP project. Our results reveal significant phylogenetic and biogeographic differences between and within the two genera. Trichodesmium exhibited greater microdiversity compared to UCYN-A, with clades showing region-specific distribution. Trichodesmium clades were primarily influenced by temperature and nutrient availability, and particularly frequent in regions of phosphorus stress. In contrast UCYN-A was found in regions of iron stress. UCYN-A clades demonstrated a more homogeneous distributions, with a single sequencing variant within the UCYN-A1 clade dominating across varied environments. The biogeographic patterns and environmental correlations of Trichodesmium and UCYN-A highlight the role of microdiversity in their ecological adaptation and reflect their different ecological strategies. This study underscores the importance of characterizing the global patterns of fine-scale genetic diversity to better understand the functional roles and distribution of marine nitrogen-fixing cyanobacteria.

microbiology↗

Intraspecific trait variation modulates the temperature effect on elemental quotas and stoichiometry in marine Synechococcus

Diverse phytoplankton modulate the coupling between the ocean carbon and nutrient cycles through life-history traits such as cell size, elemental quotas, and ratios. Biodiversity is mostly considered at broad functional levels, but major phytoplankton lineages are themselves highly diverse. As an example, Synechococcus is found in nearly all ocean regions and contain extensive intraspecific variation. Here, we grew four closely related Synechococcus isolates in semi-continuous cultures across a range of temperatures (16-25{degrees}C) to quantify for the relative role of intraspecific trait variation vs. environmental change. We report differences in cell size (p<0.01) as a function of strain and clade (p<0.01). The carbon (QC), nitrogen (QN), and phosphorus (QP) cell quotas all increased with cell size. Furthermore, cell size has an inverse relationship to growth rate. Within our experimental design, temperature alone had a weak physiological effect on cell quota and elemental ratios. Instead, we find systemic intraspecific variance of C:N:P, with cell size and N:P having an inverse relationship. Our results suggest a key role for intraspecific life history traits in determining elemental quotas and stoichiometry. Thus, the extensive biodiversity harbored within many lineages may modulate the impact of environmental change on ocean biogeochemical cycles.

ecology↗

Global scale phylogeography of functional traits and microdiversity in Prochlorococcus

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. Metagenomically 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 metagenomically 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 ecotypes 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.

microbiology↗

High spatial resolution global ocean metagenomes from Bio-GO-SHIP repeat hydrography transects

Detailed descriptions of microbial communities have lagged far behind physical and chemical measurements in the marine environment. Here, we present 720 globally distributed surface ocean metagenomes collected at high spatio-temporal resolution. Our low-cost metagenomic sequencing protocol produced 2.75 terabases of data, where the median number of base pairs per sample was 3.48 billion. The median distance between sampling stations was 26 km. The metagenomic libraries described here were collected as a part of a biological initiative for the Global Ocean Ship-based Hydrographic Investigations Program, or "Bio-GO-SHIP." One of the primary aims of GO-SHIP is to produce high spatial and vertical resolution measurements of key state variables to directly quantify climate change impacts on ocean environments. By similarly collecting marine metagenomes at high spatiotemporal resolution, we expect that this dataset will help answer questions about the link between microbial communities and biogeochemical fluxes in a changing ocean.

genomics↗

Defining trait-based microbial strategies with consequences for soil carbon cycling under climate change

Microorganisms are critical in terrestrial carbon cycling because their growth, activity and interactions with the environment largely control the fate of recent plant carbon inputs, as well as the stability of assimilated carbon (Gleixner, 2013; Schimel and Schaeffer, 2012). Soil carbon stocks reflect a balance between microbial decomposition and stabilization of organic carbon. The balance can shift under altered environmental conditions (Davidson and Janssens, 2006), and new research suggests that knowledge of microbial physiology may be critical for projecting changes in soil carbon and improving the prognosis of climate change feedbacks (Allison et al., 2010; Bradford et al., 2016; Liang et al., 2017; Wieder et al., 2015). Still, predicting the ecosystem implications of microbial processes remains a challenge. Here we argue that this challenge can be m ...

ecology↗