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At least 19 records
All sourcesNASA NTRSDOE OSTI
DOE OSTI2025

Climate-driven succession in marine microbiome biodiversity and biogeochemical function

Abstract Seasonal and El Niño-Southern Oscillation (ENSO) warming result in similar ocean changes as predicted with climate change. Climate-driven environmental cycles have strong impacts on microbiome diversity, but impacts on microbiome function are poorly understood. Here we quantify changes in microbial genomic diversity and functioning over 11 years covering seasonal and ENSO cycles at a coastal site in the southern California Current. We observe seasonal oscillations between large-genome lineages during cold, nutrient rich conditions in winter and spring versus small-genome lineages, including Prochlorococcus and Pelagibacter , in summer and fall. Parallel interannual changes separate communities depending on ENSO condition. Biodiversity shifts translate into clear oscillations in microbiome functional potential. Ocean warming induced an ecosystem with less iron but more macronutrient stress genes, depressed organic carbon degradation potential and biomass, and elevated carbon-to-nutrient biomass ratios. The consistent microbial response observed across time-scales points towards large climate-driven changes in marine ecosystems and biogeochemical cycles.

Larkin, Alyse A. (ORCID:0000000344660791)↗
DOE OSTI2020

Environmental stability impacts the differential sensitivity of marine microbiomes to increases in temperature and acidity

Ambient conditions shape microbiome responses to both short- and long-duration environment changes through processes including physiological acclimation, compositional shifts, and evolution. Here, we predict that microbial communities inhabiting locations with larger diel, episodic, and annual variability in temperature and pH should be less sensitive to shifts in these climate-change factors. To test this hypothesis, we compared responses of surface ocean microbes from more variable (nearshore) and more constant (offshore) sites to short-term factorial warming (+3 °C) and/or acidification (pH –0.3). In all cases, warming alone significantly altered microbial community composition, while acidification had a minor influence. Compared with nearshore microbes, warmed offshore microbiomes exhibited larger changes in community composition, phylotype abundances, respiration rates, and metatranscriptomes, suggesting increased sensitivity of microbes from the less-variable environment. Moreover, while warming increased respiration rates, offshore metatranscriptomes yielded evidence of thermal stress responses in protein synthesis, heat shock proteins, and regulation. Future oceans with warmer waters may enhance overall metabolic and biogeochemical rates, but they will host altered microbial communities, especially in relatively thermally stable regions of the oceans.

54 ENVIRONMENTAL SCIENCES↗
DOE OSTI2022

The microbiome of a bacterivorous marine choanoflagellate contains a resource-demanding obligate bacterial associate

Abstract Microbial predators such as choanoflagellates are key players in ocean food webs. Choanoflagellates, which are the closest unicellular relatives of animals, consume bacteria and also exhibit marked biological transitions triggered by bacterial compounds, yet their native microbiomes remain uncharacterized. Here we report the discovery of a ubiquitous, uncultured bacterial lineage we name Candidatus Comchoanobacterales ord. nov., related to the human pathogen Coxiella and physically associated with the uncultured marine choanoflagellate Bicosta minor . We analyse complete ‘Comchoano’ genomes acquired after sorting single Bicosta cells, finding signatures of obligate host-dependence, including reduction of pathways encoding glycolysis, membrane components, amino acids and B-vitamins. Comchoano encode the necessary apparatus to import energy and other compounds from the host, proteins for host-cell associations and a type IV secretion system closest to Coxiella’s that is expressed in Pacific Ocean metatranscriptomes. Interactions between choanoflagellates and their microbiota could reshape the direction of energy and resource flow attributed to microbial predators, adding complexity and nuance to marine food webs.

59 BASIC BIOLOGICAL SCIENCES↗
DOE OSTI2025

Tropical intertidal microbiome response to the 2024 Marine Honour oil spill

Marine fuel oil (MFO) spills in tropical coastal environments are under-characterized despite increasing risk from maritime activities. Microbial and geochemical responses to the June 2024 Marine Honour MFO spill on Singapore's intertidal sediments were analyzed in real time over 185 days. Using metagenomics and hydrocarbon profiling, microbial community shifts and hydrocarbon degradation were quantified across visibly oiled (high-impact) and clean (low-impact) sites. Microbiomes at all sites adapted rapidly to the spill through increased diversity and abundance of genes encoding alkane and aromatic compound degradation, detoxification, and biosurfactant production. The dominant hydrocarbon-degrading bacteria differed markedly from those reported in other crude oil spills and in regions with different climates. Oil deposition intensity strongly influenced microbial succession and hydrocarbon-degrading gene profiles, and this reflected early toxicity constraints in heavily oiled areas. The persistence of hydrocarbon degradation genes beyond hydrocarbon detection in sediments suggested long-term functional priming may occur. The study provides novel genome-resolved insight into the microbial response to MFO pollution, advances understanding of marine environmental biodegradation, and provides urgently needed baseline data for oil spill response strategies in Southeast Asia and beyond.

Coastal pollution↗
DOE OSTI2024

A global comparison of surface and subsurface microbiomes reveals large-scale biodiversity gradients, and a marine-terrestrial divide

Subsurface environments are among Earth’s largest habitats for microbial life. Yet, until recently, we lacked adequate data to accurately differentiate between globally distributed marine and terrestrial surface and subsurface microbiomes. Here, we analyzed 478 archaeal and 964 bacterial metabarcoding datasets and 147 metagenomes from diverse and widely distributed environments. Microbial diversity is similar in marine and terrestrial microbiomes at local to global scales. However, community composition greatly differs between sea and land, corroborating a phylogenetic divide that mirrors patterns in plant and animal diversity. In contrast, community composition overlaps between surface to subsurface environments supporting a diversity continuum rather than a discrete subsurface biosphere. Differences in microbial life thus seem greater between land and sea than between surface and subsurface. Diversity of terrestrial microbiomes decreases with depth, while marine subsurface diversity and phylogenetic distance to cultured isolates rivals or exceeds that of surface environments. We identify distinct microbial community compositions but similar microbial diversity for Earth’s subsurface and surface environments.

54 ENVIRONMENTAL SCIENCES↗
DOE OSTI2021

Metapangenomics reveals depth-dependent shifts in metabolic potential for the ubiquitous marine bacterial SAR324 lineage

Abstract Background Oceanic microbiomes play a pivotal role in the global carbon cycle and are central to the transformation and recycling of carbon and energy in the ocean’s interior. SAR324 is a ubiquitous but poorly understood uncultivated clade of Deltaproteobacteria that inhabits the entire water column, from ocean surface waters to its deep interior. Although some progress has been made in elucidating potential metabolic traits of SAR324 in the dark ocean, very little is known about the ecology and the metabolic capabilities of this group in the euphotic and twilight zones. To investigate the comparative genomics, ecology, and physiological potential of the SAR324 clade, we examined the distribution and variability of key genomic features and metabolic pathways in this group from surface waters to the abyss in the North Pacific Subtropical Gyre, one of the largest biomes on Earth. Results We leveraged a pangenomic ecological approach, combining spatio-temporally resolved single-amplified genome, metagenomic, and metatranscriptomic datasets. The data revealed substantial genomic diversity throughout the SAR324 clade, with distinct depth and temporal distributions that clearly differentiated ecotypes. Phylogenomic subclade delineation, environmental distributions, genomic feature similarities, and metabolic capacities revealed strong congruence. The four SAR324 ecotypes delineated in this study revealed striking divergence from one another with respect to their habitat-specific metabolic potentials. The ecotypes living in the dark or twilight oceans shared genomic features and metabolic capabilities consistent with a sulfur-based chemolithoautotrophic lifestyle. In contrast, those inhabiting the sunlit ocean displayed higher plasticity energy-related metabolic pathways, supporting a presumptive photoheterotrophic lifestyle. In epipelagic SAR324 ecotypes, we observed the presence of two types of proton-pumping rhodopsins, as well as genomic, transcriptomic, and ecological evidence for active photoheterotrophy, based on xanthorhodopsin-like light-harvesting proteins. Conclusions Combining pangenomic and both metagenomic and metatranscriptomic profiling revealed a striking divergence in the vertical distribution, genomic composition, metabolic potential, and predicted lifestyle strategies of geographically co-located members of the SAR324 bacterial clade. The results highlight the utility of metapangenomic approaches employed across environmental gradients, to decipher the properties and variation in function and ecological traits of specific phylogenetic clades within complex microbiomes.

59 BASIC BIOLOGICAL SCIENCES↗
DOE OSTI2020

Uncovering the Core Microbiome and Distribution of Palmerolide in Synoicum adareanum Across the Anvers Island Archipelago, Antarctica

Polar marine ecosystems hold the potential for bioactive compound biodiscovery, based on their untapped macro- and microorganism diversity. Characterization of polar benthic marine invertebrate-associated microbiomes is limited to few studies. This study was motivated by our interest in better understanding the microbiome structure and composition of the ascidian, Synoicum adareanum, in which palmerolide A (PalA), a bioactive macrolide with specificity against melanoma, was isolated. PalA bears structural resemblance to a hybrid nonribosomal peptide-polyketide that has similarities to microbially-produced macrolides. We conducted a spatial survey to assess both PalA levels and microbiome composition in S. adareanum in a region of the Antarctic Peninsula near Anvers Island (64°46' S, 64°03' W). PalA was ubiquitous and abundant across a collection of 21 ascidians (3 subsamples each) sampled from seven sites across the Anvers Island Archipelago. The microbiome composition (V3–V4 16S rRNA gene sequence variants) of these 63 samples revealed a core suite of 21 bacterial amplicon sequence variants (ASVs)—20 of which were distinct from regional bacterioplankton. ASV co-occurrence analysis across all 63 samples yielded subgroups of taxa that may be interacting biologically (interacting subsystems) and, although the levels of PalA detected were not found to correlate with specific sequence variants, the core members appeared to occur in a preferred optimum and tolerance range of PalA levels. These results, together with an analysis of the biosynthetic potential of related microbiome taxa, describe a conserved, high-latitude core microbiome with unique composition and substantial promise for natural product biosynthesis that likely influences the ecology of the holobiont.

59 BASIC BIOLOGICAL SCIENCES↗
DOE OSTI2025

Intestinal microbiome profile of the brown rock sea cucumber ( Holothuria glaberrima ) using ITS and 16S rDNA amplicons from direct mechanical, enzymatic, and chemical metagenomic extraction

Using direct mechanical, enzymatic, and chemical extraction methods, the intestinal microbiome of the marine invertebrate Holothuria glaberrima was obtained. ITS and 16S rDNA regions were sequenced to enrich and investigate the prokaryotic and fungal diversity profiles from different anatomical regions within the sea cucumber’s intestinal biology.

16S↗
DOE OSTI2023

The algal microbiome protects Desmodesmus intermedius from high light and temperature stress

The mutualistic impacts of bacterial communities on algal growth and biomass accumulation are well documented, but it is unknown how temperature and light stress influence these mutualistic interactions. Here, we generated a bacteria-free (axenic) culture of the green alga Desmodesmus intermedius C046 and compared its growth and yield in the laboratory to its native xenic counterpart - featuring a microbiome that has been maintained with its algal host for at least 5 years – under unstressed and high light, high temperature stress conditions. We then added exogenous microbiomes from high light marine environments to the axenic culture to quantify the contribution of these newly generated microbial consortia in improving D. intermedius growth, yield, and resilience to high light and heat. The native microbiome increased growth and biomass accumulation, under both unstressed and stressed conditions. Three of the five newly derived microbiomes had increased growth compared to the axenic and negligible, decreased, or increased growth impacts compared to the xenic culture. Stress conditions led to decreased algal exudation, larger algal cells when grown alone, but smaller algal cells with an associated microbiome. In conclusion, our results suggest that the algal microbiome plays a role in microalgal response to heat and light stress, and efforts for screening new algal strains for high biomass productivity under those stress conditions should include a strategy for microbiome optimization.

59 BASIC BIOLOGICAL SCIENCES↗
DOE OSTI2023

Herbivorous Fish Microbiome Adaptations to Sulfated Dietary Polysaccharides

Marine herbivorous fish that feed primarily on macroalgae, such as those from the genus Kyphosus, are essential for maintaining coral health and abundance on tropical reefs. Here, deep metagenomic sequencing and assembly of gut compartment-specific samples from three sympatric, macroalgivorous Hawaiian kyphosid species have been used to connect host gut microbial taxa with predicted protein functional capacities likely to contribute to efficient macroalgal digestion. Bacterial community compositions, algal dietary sources, and predicted enzyme functionalities were analyzed in parallel for 16 metagenomes spanning the mid- and hindgut digestive regions of wild-caught fishes. Gene colocalization patterns of expanded carbohydrate (CAZy) and sulfatase (SulfAtlas) digestive enzyme families on assembled contigs were used to identify likely polysaccharide utilization locus associations and to visualize potential cooperative networks of extracellularly exported proteins targeting complex sulfated polysaccharides. These insights into the gut microbiota of herbivorous marine fish and their functional capabilities improve our understanding of the enzymes and microorganisms involved in digesting complex macroalgal sulfated polysaccharides.

09 BIOMASS FUELS↗
DOE OSTI2023

Biotic countermeasures that rescue Nannochloropsis gaditana from a Bacillus safensis infection

The natural assemblage of a symbiotic bacterial microbiome (bacteriome) with microalgae in marine ecosystems is now being investigated as a means to increase algal productivity for industry. When algae are grown in open pond settings, biological contamination causes an estimated 30% loss of the algal crop. Therefore, new crop protection strategies that do not disrupt the native algal bacteriome are needed to produce reliable, high-yield algal biomass. Bacteriophages offer an unexplored solution to treat bacterial pathogenicity in algal cultures because they can eliminate a single species without affecting the bacteriome. To address this, we identified a highly virulent pathogen of the microalga Nannochloropsis gaditana, the bacterium Bacillus safensis, and demonstrated rescue of the microalgae from the pathogen using phage. 16S rRNA amplicon sequencing showed that phage treatment did not alter the composition of the bacteriome. It is widely suspected that the algal bacteriome could play a protective role against bacterial pathogens. To test this, we compared the susceptibility of a bacteriome-attenuated N. gaditana culture challenged with B. safensis to a N. gaditana culture carrying a growth-promoting bacteriome. We showed that the loss of the bacteriome increased the susceptibility of N. gaditana to the pathogen. Transplanting the microalgal bacteriome to the bacteriome-attenuated culture reconstituted the protective effect of the bacteriome. Finally, the success of phage treatment was dependent on the presence of beneficial bacteriome. This study introduces two synergistic countermeasures against bacterial pathogenicity in algal cultures and a tractable model for studying interactions between microalgae, phages, pathogens, and the algae microbiome.

60 APPLIED LIFE SCIENCES↗
DOE OSTI2024

Non-photosynthetic lineages sibling to Cyanobacteria associate with eukaryotes in the open ocean

Margulisbacteria are elusive uncultivated bacteria that have illuminated evolutionary transitions in the progenitor of Cyanobacteria, the latter being a critically important phylum that underpins oxygenic photosynthesis. The non-photosynthetic Margulisbacteria were discovered in a sulfidic spring and later in other habitats. Currently, this candidate phylum partitions into the Riflemargulisbacteria, primarily from sediments and groundwater, the Termititenax from insect gut microbiomes, and the Marinamargulisbacteria, from marine samples. We found that Marinamargulisbacteria amplicons were unusually distributed in size-fractionated samples from the sunlit photic and dark twilight zones of the ocean. Further, sequencing of wild marine protists rendered genomic information for distinct marinamargulisbacterial clades co-associated with uncultivated, non-photosynthetic Stramenopila and Opisthokonta protists. Phylogenomic analyses combining these data and available metagenome-assembled genomes (MAGs) and single-amplified genomes (SAGs) from sorted bacteria revealed new Marinamargulisbacteria lineages. The lineages delineate by their environment, forming clades comprising freshwater, marine pelagic, or sediment/hypoxic taxa. In conclusion, the remarkable diversity of Margulisbacteria indicates success in colonizing various habitats, potentially in a conserved strategy involving eukaryotic cells.

59 BASIC BIOLOGICAL SCIENCES↗
DOE OSTI2021

Global Diversity and Biogeography of the Zostera marina Mycobiome

Seagrasses are marine flowering plants that provide critical ecosystem services in coastal environments worldwide. Marine fungi are often overlooked in microbiome and seagrass studies, despite terrestrial fungi having critical functional roles as decomposers, pathogens, or endophytes in global ecosystems. Here, we characterize the distribution of fungi associated with the seagrass Zostera marina, using leaves, roots, and rhizosphere sediment from 16 locations across its full biogeographic range. Using high-throughput sequencing of the ribosomal internal transcribed spacer (ITS) region and 18S rRNA gene, we first measured fungal community composition and diversity. We then tested hypotheses of neutral community assembly theory and the degree to which deviations suggested that amplicon sequence variants (ASVs) were plant selected or dispersal limited. Finally, we identified a core mycobiome and investigated the global distribution of differentially abundant ASVs. We found that the fungal community is significantly different between sites and that the leaf mycobiome follows a weak but significant pattern of distance decay in the Pacific Ocean. Generally, there was evidence for both deterministic and stochastic factors contributing to community assembly of the mycobiome, with most taxa assembling through stochastic processes. The Z. marina core leaf and root mycobiomes were dominated by unclassified Sordariomycetes spp., unclassified Chytridiomycota lineages (including Lobulomycetaceae spp.), unclassified Capnodiales spp., and Saccharomyces sp. It is clear from the many unclassified fungal ASVs and fungal functional guilds that knowledge of marine fungi is still rudimentary. Further studies characterizing seagrass-associated fungi are needed to understand the roles of these microorganisms generally and when associated with seagrasses. Fungi have important functional roles when associated with land plants, yet very little is known about the roles of fungi associated with marine plants, like seagrasses. In this study, we report the results of a global effort to characterize the fungi associated with the seagrass Zostera marina across its full biogeographic range. Although we defined a putative global core fungal community, it is apparent from the many fungal sequences and predicted functional guilds that had no matches to existing databases that general knowledge of seagrass-associated fungi and marine fungi is lacking. This work serves as an important foundational step toward future work investigating the functional ramifications of fungi in the marine ecosystem.

ITS2↗
DOE OSTI2023

MetaboDirect: an analytical pipeline for the processing of FT-ICR MS-based metabolomic data

Background: Microbiomes are now recognized as the main drivers of ecosystem function ranging from the oceans and soils to humans and bioreactors. However, a grand challenge in microbiome science is to characterize and quantify the chemical currencies of organic matter (i.e., metabolites) that microbes respond to and alter. Critical to this has been the development of Fourier transform ion cyclotron resonance mass spectrometry (FT-ICR MS), which has drastically increased molecular characterization of complex organic matter samples, but challenges users with hundreds of millions of data points where readily available, user-friendly, and customizable software tools are lacking. Results: Here, we build on years of analytical experience with diverse sample types to develop MetaboDirect, an open-source, command-line-based pipeline for the analysis (e.g., chemodiversity analysis, multivariate statistics), visualization (e.g., Van Krevelen diagrams, elemental and molecular class composition plots), and presentation of direct injection high-resolution FT-ICR MS data sets after molecular formula assignment has been performed. When compared to other available FT-ICR MS software, MetaboDirect is superior in that it requires a single line of code to launch a fully automated framework for the generation and visualization of a wide range of plots, with minimal coding experience required. Among the tools evaluated, MetaboDirect is also uniquely able to automatically generate biochemical transformation networks (ab initio) based on mass differences (mass difference network-based approach) that provide an experimental assessment of metabolite connections within a given sample or a complex metabolic system, thereby providing important information about the nature of the samples and the set of microbial reactions or pathways that gave rise to them. Finally, for more experienced users, MetaboDirect allows users to customize plots, outputs, and analyses. Conclusion: Application of MetaboDirect to FT-ICR MS-based metabolomic data sets from a marine phage-bacterial infection experiment and a Sphagnum leachate microbiome incubation experiment showcase the exploration capabilities of the pipeline that will enable the research community to evaluate and interpret their data in greater depth and in less time. It will further advance our knowledge of how microbial communities influence and are influenced by the chemical makeup of the surrounding system. The source code and User’s guide of MetaboDirect are freely available through (https://github.com/Coayala/MetaboDirect) and (https://metabodirect.readthedocs.io/en/latest/), respectively.

54 ENVIRONMENTAL SCIENCES↗
DOE OSTI2021

Evaluating a Laboratory Flume Microbiome as a Window Into Natural Riverbed Biogeochemistry

Riverbeds are hotspots for microbially-mediated reactions that exhibit pronounced variability in space and time. It is challenging to resolve biogeochemical mechanisms in natural riverbeds, as uncontrolled settings complicate data collection and interpretation. To overcome these challenges, laboratory flumes are often used as proxies for natural riverbed systems. Flumes capture spatiotemporal variability and thus allow for controlled investigations of riverbed biogeochemistry. These investigations implicitly rely on the assumption that the flume microbiome is similar to the microbiome of natural riverbeds. However, this assumption has not been tested and it is unknown how the microbiome of a flume compares to natural aquatic settings, including riverbeds. To evaluate the fundamental assumption that a flume hosts a microbiome similar to natural riverbed systems, we used 16s rRNA gene sequencing and publicly available data to compare the sediment microbiome of a single large laboratory flume to a wide variety of natural ecosystems including lake and marine sediments, river, lake, hyporheic, soil, and marine water, and bank and wetland soils. Richness and Shannon diversity metrics, analyses of variance, Bray-Curtis dissimilarity, and analysis of the common microbiomes between flume and river sediment all indicated that the flume microbiome more closely resembled natural riverbed sediments than other ecosystems, supporting the use of flume experiments for investigating natural microbially-mediated biogeochemical processes in riverbeds.

54 ENVIRONMENTAL SCIENCES↗
DOE OSTI2020

Reused cultivation water from a self-inhibiting alga does not inhibit other algae but alters their microbiomes

Economical production of algal commodities (food, feed, and fuels) requires reusing cultivation water to reduce operating costs. While some algae strains show growth inhibition in reused water, other strains appear un-affected. Reusing water to grow different strains (i.e., crop rotation) could potentially improve overall biomass production compared to water reuse with the same strain by reducing accumulation of strain-specific waste products, limiting carryover of population-specific pathogens such as viruses, and introducing bacteria that degrade residual organic matter. Here, batch culture experiments tested the effects of reused cultivation water from the self-inhibiting diatom Staurosira sp. C323 on the diatom Navicula sp. SFP and green alga Chlorella sp. D046, as well as their microbiomes. Navicula sp. and Chlorella sp. grew well in Staurosira sp. reused water, indicating that previously observed self-inhibition was likely specific to this Staurosira strain. While algal mi-crobiomes were not significantly different between controls and reused water treatments, specific bacteria taxa were differentially abundant in reused treatments, suggesting that some taxa responded to compounds re-maining in the reused water. Finally, results suggest that algae growth responses in reused water may depend largely on strain-specific factors, and that crop rotation can support biomass production.

09 BIOMASS FUELS↗
DOE OSTI2024

Sponge exhalent metabolites influence coral reef picoplankton dynamics

Coral reef sponges efficiently take up particulate and dissolved organic matter (DOM) from the water column and release compounds such as nucleosides, amino acids, and other dissolved metabolites to the surrounding reef via their exhalent seawater, but the influence of this process on reef picoplankton and nutrient processing is relatively unexplored. Here we examined the impact of sponge exhalent on the reef picoplankon community and subsequent alterations to the reef dissolved metabolite pool. We exposed reef picoplankton communities to a sponge exhalent water mixture (Niphates digitalis and Xestospongia muta) or filtered reef seawater (control) in closed, container-based dark incubations. We used 16S rRNA gene sequencing and flow cytometry-based cell counts to examine the picoplankton community and metabolomics and other analyses to examine the dissolved metabolite pool. The initial sponge exhalent was enriched in adenosine, inosine, chorismate, humic-like and amino acid-like components, and ammonium. Following 48 h of exposure to sponge exhalent, the picoplankton differed in composition, were reduced in diversity, showed doubled (or higher) growth efficiencies, and harbored increased copiotrophic and denitrifying taxa (Marinomonas, Pontibacterium, Aliiroseovarius) compared to control, reef-water based incubations. Alongside these picoplankton alterations, the sponge treatments, relative to seawater controls, had decreased adenosine, inosine, tryptophan, and ammonium, metabolites that may support the observed higher picoplankton growth efficiencies. Sponge treatments also had a net increase in several monosaccharides and other metabolites including anthranilate, riboflavin, nitrite, and nitrate. Our work demonstrates a link between sponge exhalent-associated metabolites and the picoplankton community, with exhalent water supporting an increased abundance of efficient, copiotrophic taxa that catabolize complex nutrients. The copiotrophic taxa were often different from those observed in previous algae and coral studies. These results have implications for better understanding the multifaceted role of sponges on picoplankton biomass with subsequent potential impacts to coral and other planktonic feeders in oligotrophic reef environments.

59 BASIC BIOLOGICAL SCIENCES↗