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Biology subjects

Guidi, L.

Publications and source records attributed to Guidi, L..

12 recordsLinked to original sources

Satellite-gene abundance fusion reveals global hotspots of ocean ecosystem services

The Ocean sustains planetary health through climate regulation, biodiversity, and essential ecosystem services. Plankton underpins these processes by driving primary production, sustaining food webs, and mediating carbon sequestration. Yet the spatial organization of plankton-based ecosystem services remains poorly understood. The High Seas Treaty and the 30% Ocean protection target by 2030 create an urgent need for science-based guidance for global ocean governance. Here, we aim to identify key planktonic areas associated with functional diversity, net primary productivity, and carbon export globally. We used machine learning to integrate omics-derived plankton functions and satellite observations with diversity metric and ecosystem services. Leveraging metagenomic data, we identified molecular functions strongly linked to ecosystem functioning and project their global distributions across seasons. We reveal putative hotspots of functional diversity, net primary productivity, and carbon export. Our analysis pinpoints areas where all three indicators converge synchronously, predominantly along oceanographic structures such as polar fronts and principal current systems. By relying on satellite data as core input, our approach captures the temporal variability of these hotspots, providing a global, dynamic protocol for projections of plankton-based ecosystem services. These findings establish a foundation for developing integrative conservation tools based on ecosystem functioning and inform adaptive management under climate change.

ecology↗

Global pattern of nitrogen metabolism in marine prokaryotes

The ocean nitrogen cycle is driven by an ensemble of metabolic processes sustaining marine ecosystems and ocean productivity. However, the spatial distribution and environmental drivers of its major pathways, i.e., nitrogen fixation, denitrification, assimilatory and dissimilatory nitrate reduction to ammonium (ANRA, DNRA), and nitrification are not well known. Furthermore, the taxonomic composition of the prokaryotes supporting each pathway remain incompletely understood. Leveraging newly assembled global marine metagenomic datasets and a state-of-the-art machine learning framework, we inferred the global biogeography of the genomic potential for key metabolic pathways of the marine nitrogen cycle. This was achieved using a multi-output regression of gene read counts against environmental climatologies. Our results reveal distinct biogeographic patterns of genomic potential: anaerobic or light-inhibited pathways are enriched in high-latitude regions, eastern boundary upwelling systems, and deeper ocean layers, while nitrogen fixation and ANRA dominate in oligotrophic gyres. These patterns are consistent with known metabolic strategies, model-based estimates, and underlying taxonomy. Indeed, we identify that Cyanobacteria associate primarily with aerobic, biosynthetic pathways, while Gammaproteobacteria and Nitrososphaeria encode for nitrogen transformations related to energy requirements. By coupling microbial community composition with genome-level information, our approach advances understanding of the microbial foundations of nitrogen transformation pathways and offers new insights on underrepresented processes into biogeochemical models. We highlight the growing value of omic data to better understand marine ecosystem function in relation to environmental gradients and community composition, and their use as a potential observation-based alternative or complement to biogeochemical models.

biochemistry↗

Planetary-scale marine community modeling predicts metabolic synergy and viral impacts

The oceans buffer against climate change via biogeochemical cycles underpinned by microbial metabolic activities. While planetary-scale surveys provide baseline microbiome data, inferring metabolic and biogeochemical impacts remains challenging. Genome-scale modeling has addressed analogous issues at the cellular level, highlighting key metabolic reactions contingent upon specific environmental conditions. Here we adapt this mechanistic modeling framework towards analyzing global ocean microbial communities to reveal metabolic processes predicted to maintain ecosystem functioning. To achieve this, we developed a genome-scale superorganism metabolic model for each TARA Ocean metagenome or metatranscriptome (i.e., limited to reactions known from heterotrophic prokaryotes and viruses), and evaluated these models to establish a community-wide metabolic phenotype for each sample. To validate, we showed that even with reaction-mappable genes only ([~]1/4 of the total genes), model composition revealed metabolism-inferred ecological zones that matched taxonomy-inferred zones. Model inferred metabolic phenotypes revealed reaction cooperation associated with microbial metabolism and organism diversity. These phenotypes also suggest elevated ecological roles for viruses as model predictions suggest they genomically target community-critical metabolic reactions that underpin metabolic phenotype stability, and also demonstrate that, as metabolites are better understood, immediate estimates could be made for where viruses remineralize versus sink carbon. While this new constraints-based, agile, and mechanistic modeling framework is highly upgradable, it already begins to convert molecular-scale environmental omics data to ecological and even planetary-scale biogeochemical features that will better bring microbes and their viruses into Earth system and climate models.

systems biology↗

Cortical layer 6b mediates state-dependent changes in brain activity and effects of orexin on waking and sleep

One of the most distinctive features of the mammalian cerebral cortex is its laminar structure. Of all cortical layers, layer 6b (L6b) is by far the least-studied, despite exhibiting direct sensitivity to orexin and having widespread connectivity, suggesting an important role in regulating cortical oscillations and brain state. We performed chronic electroencephalogram (EEG) recordings in mice in which a subset of L6b neurons was conditionally "silenced", during undisturbed conditions, after sleep deprivation (SD), and after intracerebroventricular (ICV) administration of orexin. While the total amount of waking and sleep or the response to SD were not altered, L6b-silenced mice showed a slowing of theta frequency (6-9 Hz) during wake and REM sleep, and a marked reduction of total EEG power, especially in NREM sleep. The infusion of orexin A increased wakefulness in both genotypes, but subsequent levels of EEG slow-wave activity during NREM sleep were lower in L6b-silenced animals in the occipital derivation. In summary, these results demonstrate a role for cortical L6b in state-dependent brain oscillations and in the response to orexinergic neurotransmission. Our findings provide new insights in functions of L6b neurons and could inform the understanding of abnormal regulation of brain states in neurodevelopmental and psychiatric disorders.

neuroscience↗

An orexin-sensitive subpopulation of layer 6 neurons regulates cortical excitability and anxiety behaviour.

Cortical layer 6 (L6) neurons uniquely respond to orexin - a neuropeptide influencing arousal and emotion. We show that Drd1a-Cre+ neurons in the prefrontal cortex are selectively sensitive to orexin and regulate prefrontal network activation in vitro and in vivo. Chronically silencing these neurons impairs orexin-induced prefrontal activation and reduces anxiety-like behaviour, indicating that orexin-responsive L6 neurons modulate emotional states and may be a substrate for anxiety regulation.

neuroscience↗

Ubiquity of inverted 'gelatinous' ecosystem pyramids in the global ocean

Summary paragraphPlankton are essential in marine ecosystems. However, our knowledge of overall community structure is sparse due to inconsistent sampling across their very large organismal size range. Here we use diverse imaging methods to establish complete plankton inventories of organisms spanning five orders of magnitude in size. Plankton community size and trophic structure variation validate a long-held theoretical link between organism size-spectra and ecosystem trophic structures. We found that predator/grazer biomass and biovolume unexpectedly exceed that of primary producers at most (55%) locations, likely due to our better quantification of gelatinous organisms. Bottom- heavy ecosystems (the norm on land) appear to be rare in the ocean. Collectively, gelatinous organisms represent 30% of the total biovolume (8-9% of carbon) of marine plankton communities from tropical to polar ecosystems. Communities can be split into three extreme typologies: diatom/copepod-dominated in eutrophic blooms, rhizarian/chaetognath-dominated in oligotrophic tropical oceans, and gelatinous-dominated elsewhere. While plankton taxonomic composition changes with latitude, functional and trophic structures mostly depend on the amount of prey available for each trophic level. Given future projections of oligotrophication of marine ecosystems, our findings suggest that rhizarian and gelatinous organisms will increasingly dominate the apex position of planktonic ecosystems, leading to significant changes in the oceans carbon cycle.

ecology↗

Towards modeling genome-scale knowledge in the global ocean

Earth System Models (ESMs) highly simplify their representation of biological processes, leading to major uncertainty in climate change impacts. Despite a growing understanding of molecular networks from genomic data, describing how changing phytoplankton physiology affects the production of key metabolites remains elusive. Here we embed a genome-scale model within a state-of-the-art ESM to deliver an integrated understanding of how gradients of nutritional constraints modulate metabolic reactions and molecular physiology. Applied to the prevalent marine cyanobacteria Prochlorococcus, we find that glycogen and lipid storage can be understood as a consequence of acclimation to environmental gradients. Given the pressing need to assess how biological diversity influences biogeochemical functions, genome-enabled ESMs allow the quantification of the contribution of modeled organisms to the production of dissolved organic carbon and its molecular composition.

bioinformatics↗

Picoeukaryotic photosynthetic potential is functionally redundant but taxonomically structured at global scale

Primary production, performed by RUBISCO, and often associated with carbon concentration mechanisms, is of major importance in the oceans. Thanks to growing metagenomic resources (e.g., eukaryotic Metagenome-Assembled-Genomes; MAGs), we provide the first reproducible machine-learning-based framework to derive the potential biogeography of a given function, through the multi-output regression of the standardized number of reads of the associated genes on environmental climatologies. We use it to study the genomic potential of C4-photosynthesis of picoeukaryotes, a diverse and abundant group of marine unicellular photosynthetic organisms. We show that the genomic potential supporting C4-enzymes and RUBISCO exhibit strong functional redundancy and an important affinity towards tropical oligotrophic waters. This redundancy is then structured taxonomically by the dominance of Mamiellophyceae and Prymnesiophyceae in mid and high latitudes. Finally, unlike the genomic potential related to most C4-enzymes, the one of RUBISCO showed a clear pattern affinity for temperate waters.

ecology↗

Loss of the benthic life stage in Medusozoa and colonization of the open ocean

In marine environments, life cycle strategies strongly impact species dispersal and their ability to colonize new habitats. Pelagic medusozoans (jellyfish and siphonophores) exhibit various reproductive strategies, variations of meroplanktonic and holoplanktonic life cycles. In the ancestral meroplanktonic life cycle, a benthic polyp stage alternates with a pelagic medusa stage. During the course of evolution, some medusozoans lost their benthic stage, leading to a holoplanktonic life cycle. The ecological consequences of these losses have not been addressed at global scale. Here, integrating metabarcoding and environmental data from Tara Oceans into a phylogenetic framework, we show that each convergent transition toward a holoplanktonic life cycle is associated with a more offshore distribution compared to meroplanktonic medusozoans. Our analyses showed that holoplanktonic medusozoans are more globally distributed and relatively more abundant than meroplanktonic medusozoans, although they are less diversified and occupy a more peripheral position in a global plankton community interactome. This suggests that holoplanktonic medusozoans have acquired a greater tolerance to biotic and abiotic conditions. Overall, our results demonstrate the relationship between medusozoan life cycles, distribution, and biotic interactions, suggesting that the loss of the benthic stage promoted colonization of the open ocean.

evolutionary biology↗

Global observation of plankton communities from space

Satellite remote sensing from space is a powerful way to monitor the global dynamics of marine plankton. Previous research has focused on developing models to predict the size or taxonomic groups of phytoplankton. Here we present an approach to identify representative communities from a global plankton network that included both zooplankton and phytoplankton and using global satellite observations to predict their biogeography. Six representative plankton communities were identified from a global co-occurrence network inferred using a novel rDNA 18S V4 planetary-scale eukaryotic metabarcoding dataset. Machine learning techniques were then applied to train a model that predicted these representative communities from satellite data. The model showed an overall 67% accuracy in the prediction of the representative communities. The prediction based on 17 satellite-derived parameters showed better performance than based only on temperature and/or the concentration of chlorophyll a. The trained model allowed to predict the global spatiotemporal distribution of communities over 19-years. Our model exhibited strong seasonal changes in the community compositions in the subarctic-subtropical boundary regions, which were consistent with previous field observations. This network-oriented approach can easily be extended to more comprehensive models including prokaryotes as well as viruses.

ecology↗

Genomic evidence for global ocean plankton biogeography shaped by large-scale current systems

Biogeographical studies have traditionally focused on readily visible organisms, but recent technological advances are enabling analyses of the large-scale distribution of microscopic organisms, whose biogeographical patterns have long been debated. Here we assessed the global structure of plankton geography and its relation to the biological, chemical and physical context of the ocean (the seascape) by analyzing metagenomes of plankton communities sampled across oceans during the Tara Oceans expedition, in light of environmental data and ocean current transport. Using a consistent approach across organismal sizes that provides unprecedented resolution to measure changes in genomic composition between communities, we report a pan-ocean, size-dependent plankton biogeography overlying regional heterogeneity. We found robust evidence for a basin-scale impact of transport by ocean currents on plankton biogeography, and on a characteristic timescale of community dynamics going beyond simple seasonality or life history transitions of plankton.

ecology↗

Viruses of the eukaryotic plankton are predicted to increase carbon export efficiency in the global sunlit ocean

The biological carbon pump, in which carbon fixed by photosynthesis is exported to the deep ocean through sinking, is a major process in Earths carbon cycle. The proportion of primary production that is exported is termed the carbon export efficiency (CEE). Based on in-lab or regional scale observations, viruses were previously suggested to affect the CEE (i.e., viral "shunt" and "shuttle"). In this study, we tested associations between viral community composition and CEE measured at a global scale. A regression model based on relative abundance of viral marker genes explained 67% of the variation in CEE. Viruses with high importance in the model were predicted to infect ecologically important hosts. These results are consistent with the view that the viral shunt and shuttle functions at a large scale and further imply that viruses likely act in this process in a way dependent on their hosts and ecosystem dynamics.

ecology↗