Resource partitioning of phytoplankton metabolites that support bacterial heterotrophy.
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ABSTRACT:
SUBMITTER: Ferrer-Gonzalez FX
PROVIDER: S-EPMC8027193 | biostudies-literature |
REPOSITORIES: biostudies-literature
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Project description:<p>The communities of marine bacteria that assemble around living microphytoplankton are predictably dominated by three taxonomic groups, each of which specializes in the use or transport of different components of the available metabolite pool: Rhodobacterales transport small and polar metabolites, Flavobacteriia use carbohydrate-rich polymers, and Gammaproteobacteria use compounds from both classes. The consistent ecological pattern involving these three taxa is widespread throughout the surface ocean, yet whether it reflects the outcome competition or niche partitioning of the phytoplankton-derived compounds is not clear. Addressing this question requires better knowledge than currently exists of the metabolites that link microbial autotrophs and heterotrophs in the surface ocean. Here we used two untargeted biological screening strategies that leverage bacterial proficiency for scavenging dilute substrates from chemically complex mixtures to characterize metabolite uptake by heterotrophic bacteria. In the first, expression patterns of transporters and diagnostic catabolic genes were analyzed in model marine bacteria grown individually in co-culture with the diatom Thalassiosira pseudonana. In the second, the ability of bacteria to draw down exometabolites from the culture medium was detected by novel approaches in mass spectrometry (MS) and nuclear magnetic resonance (NMR) analysis. These methods identified diverse chemical currencies mediating carbon transfer including low molecular weight metabolites (nucleosides, amino acids, organic acids, monomeric sugars, peptides, and sulfonates) and components of polysaccharides (chrysolaminarin, chitin oligomers, and alginate-like oligosaccharides). Bacterial utilization of bioreactive metabolites in the absence of competition indicated low resource overlap among strains and a dominance of resource partitioning over resource competition among the bacterial groups that process a major fraction of marine net primary production.</p><p><br></p><p><strong>NMR assay</strong> is reported in the current study <a href='https://www.ebi.ac.uk/metabolights/MTBLS1544' rel='noopener noreferrer' target='_blank'><strong>MTBLS1544</strong></a></p><p><strong>UPLC-MS assay</strong> is reported in <a href='https://www.ebi.ac.uk/metabolights/MTBLS1751' rel='noopener noreferrer' target='_blank'><strong>MTBLS1751</strong></a></p>
2020-09-15 | MTBLS1544 | MetaboLights
Project description:<p>The communities of marine bacteria that assemble around living microphytoplankton are predictably dominated by three taxonomic groups, each of which specializes in different components of the available metabolite pool: Rhodobacterales transport small and polar metabolites, Flavobacteriia use carbohydrate-rich polymers, and Gammaproteobacteria use compounds from both classes. The consistent ecological pattern involving these three taxa is widespread throughout the surface ocean, yet whether it reflects the outcome competition or niche partitioning of the phytoplankton-derived compounds is not clear. Addressing this question requires better knowledge than currently exists of the metabolites that link microbial autotrophs and heterotrophs in the surface ocean. Here we used two untargeted biological screening strategies that leverage bacterial proficiency for scavenging dilute substrates from chemically complex mixtures to characterize metabolite uptake by heterotrophic bacteria. In the first, expression patterns of transporters and diagnostic catabolic genes were analyzed in model marine bacteria grown individually in co-culture with the diatom Thalassiosira pseudonana. In the second, the ability of bacteria to draw down exometabolites from the culture medium was detected by novel approaches in mass spectrometry (MS) and nuclear magnetic resonance (NMR) analysis. These methods identified diverse chemical currencies mediating carbon transfer including low molecular weight metabolites (nucleosides, amino acids, organic acids, monomeric sugars, peptides, and sulfonates) and components of polysaccharides (chrysolaminarin, chitin oligomers, and alginate-like oligosaccharides). Bacterial utilization of bioreactive metabolites in the absence of competition indicated low resource overlap among strains and a dominance of resource partitioning over resource competition among the bacterial groups that process a major fraction of marine net primary production.</p><p><br></p><p><strong>UPLC-MS assay</strong> is reported in the current study <a href='https://www.ebi.ac.uk/metabolights/MTBLS1751' rel='noopener noreferrer' target='_blank'><strong>MTBLS1751</strong></a></p><p><strong>NMR assay</strong> is reported in <a href='https://www.ebi.ac.uk/metabolights/MTBLS1544' rel='noopener noreferrer' target='_blank'><strong>MTBLS1544</strong></a></p>
2020-09-15 | MTBLS1751 | MetaboLights
Project description:Blooms of nitrogen-fixing cyanobacteria are recurrent phenomena in marine and freshwater habitats, and their supplying role in aquatic biogeochemical cycles is generally considered vital. The objective of this study was to analyse whether an increasing proportion of nitrogen-fixing cyanobacteria affects (i) the composition of the non-diazotrophic component of ambient phytoplankton communities and (ii) resource use efficiency (RUE; ratio of Chl a to total nutrients) - an important ecosystem function. We hypothesize that diazotrophs increase community P use and decrease N use efficiencies, as new N is brought into the system, relaxing N, and concomitantly aggravating P limitation. We test this by analysing an extensive data set from the Baltic Sea (> 3700 quantitative phytoplankton samples), known to harbour conspicuous and recurrent blooms of Nodularia spumigena and Aphanizomenon sp.System-level phosphorus use efficiency (RUEP) was positively related to high proportion of diazotrophic cyanobacteria, suggesting aggravation of phosphorus limitation. However, concomitant decrease of nitrogen use efficiency (RUEN) was not observed. Nodularia spumigena, a dominant diazotroph and a notorious toxin producer, had a significantly stronger relationship with RUEP, compared to the competing non-toxic Aphanizomenon sp., confirming niche differentiation in P acquisition strategies between the major bloom-forming cyanobacterial species in the Baltic Sea. Nodularia occurrences were associated with stronger temperature stratification in more offshore environments, indicating higher reliance on in situ P regeneration.By using constrained and unconstrained ordination, permutational multivariate analysis of variance and local similarity analysis, we show that diazotrophic cyanobacteria explained no more than a few percentage of the ambient phytoplankton community variation. The analyses furthermore yielded rather evenly distributed negative and positive effects on individual co-occurring phytoplankton taxa, with no obvious phylogenetic or functional trait-based patterns. Synthesis. Our study reveals that despite the widely acknowledged noxious impacts of cyanobacterial blooms, the overall effect on phytoplankton community structure is minor. There are no predominantly positive or negative associations with ambient phytoplankton species. Species-specific niche differences in cyanobacterial resource acquisition affect important ecosystem functions, such as biomass production per unit limiting resource.
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Project description:The microenvironment surrounding individual phytoplankton cells is often rich in dissolved organic matter (DOM), which can attract bacteria by chemotaxis. These "phycospheres" may be prominent sources of resource heterogeneity in the ocean, affecting the growth of bacterial populations and the fate of DOM. However, these effects remain poorly quantified due to a lack of quantitative ecological frameworks. Here, we used video microscopy to dissect with unprecedented resolution the chemotactic accumulation of marine bacteria around individual Chaetoceros affinis diatoms undergoing lysis. The observed spatiotemporal distribution of bacteria was used in a resource utilization model to map the conditions under which competition between different bacterial groups favors chemotaxis. The model predicts that chemotactic, copiotrophic populations outcompete nonmotile, oligotrophic populations during diatom blooms and bloom collapse conditions, resulting in an increase in the ratio of motile to nonmotile cells and in the succession of populations. Partitioning of DOM between the two populations is strongly dependent on the overall concentration of bacteria and the diffusivity of different DOM substances, and within each population, the growth benefit from phycospheres is experienced by only a small fraction of cells. By informing a DOM utilization model with highly resolved behavioral data, the hybrid approach used here represents a new path toward the elusive goal of predicting the consequences of microscale interactions in the ocean.
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Project description:In shade-intolerant plants, the perception of proximate neighbors rapidly induces architectural changes resulting in elongated stems and reduced leaf size. Sensing and signaling steps triggering this modified growth program have been identified. However, the underlying changes in resource allocation that fuel stem growth remain poorly understood. Through 14CO2 pulse labeling of Brassica rapa seedlings, we show that perception of the neighbor detection signal, low ratio of red to far-red light (R:FR), leads to increased carbon allocation from the major site of photosynthesis (cotyledons) to the elongating hypocotyl. While carbon fixation and metabolite levels remain similar in low R:FR, partitioning to all downstream carbon pools within the hypocotyl is increased. Genetic analyses using Arabidopsis thaliana mutants indicate that low-R:FR-induced hypocotyl elongation requires sucrose transport from the cotyledons and is regulated by a PIF7-dependent metabolic response. Moreover, our data suggest that starch metabolism in the hypocotyl has a growth-regulatory function. The results reveal a key mechanism by which metabolic adjustments can support rapid growth adaptation to a changing environment.
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Project description:Herbivores are major drivers of ecosystem structure, diversity, and function. Resilient ecosystems therefore require viable herbivore populations in a sustainable balance with environmental resource availability. This balance is becoming harder to achieve, with increasingly threatened species reliant on small protected areas in increasingly harsh and unpredictable environments. Arid environments in North Africa exemplify this situation, featuring a biologically distinct species assemblage exposed to extreme and volatile conditions, including habitat loss and climate change-associated threats. Here, we implement an integrated likelihood approach to relate scimitar-horned oryx (Oryx dammah) and dorcas gazelle (Gazella dorcas) density, via dung distance sampling, to habitat, predator, and geographic correlates in Dghoumes National Park, Tunisia. We show how two threatened sympatric ungulates partition resources on the habitat axis, exhibiting nonuniform responses to the same vegetation gradient. Scimitar-horned oryx were positively associated with plant species richness, selecting for vegetated ephemeral watercourses (wadis) dominated by herbaceous cover. Conversely, dorcas gazelle were negatively associated with vegetation density (herbaceous height, litter cover, and herbaceous cover), selecting instead for rocky plains with sparse vegetation. We suggest that adequate plant species richness should be a prerequisite for areas proposed for future ungulate reintroductions in arid and semi-arid environments. This evidence will inform adaptive management of reintroduced ungulates in protected environments, helping managers and planners design sustainable ecosystems and effective conservation programs.
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Project description:Every evening, from late spring to mid-summer, tens of thousands of hungry lactating female lesser long-nosed bats (Leptonycteris yerbabuenae) emerge from their roost and navigate over the Sonoran Desert, seeking for nectar and pollen [1, 2]. The bats roost in a huge maternal colony that is far from the foraging grounds but allows their pups to thermoregulate [3] while the mothers are foraging. Thus, the mothers have to fly tens of kilometers to the foraging sites-fields with thousands of Saguaro cacti [4, 5]. Once at the field, they must compete with many other bats over the same flowering cacti. Several solutions have been suggested for this classical foraging task of exploiting a resource composed of many renewable food sources whose locations are fixed. Some animals randomly visit the food sources [6], and some actively defend a restricted foraging territory [7-11] or use simple forms of learning, such as "win-stay lose-switch" strategy [12]. Many species have been suggested to follow a trapline, that is, to revisit the food sources in a repeating ordered manner [13-22]. We thus hypothesized that lesser long-nosed bats would visit cacti in a sequenced manner. Using miniature GPS devices, aerial imaging, and video recordings, we tracked the full movement of the bats and all of their visits to their natural food sources. Based on real data and evolutionary simulations, we argue that the bats use a reinforcement learning strategy that requires minimal memory to create small, non-overlapping cacti-cores and exploit nectar efficiently, without social communication.
| S-EPMC7575196 | biostudies-literature
Project description:Unlike biologically available nitrogen and phosphorus, which are often at limiting concentrations in surface seawater, sulfur in the form of sulfate is plentiful and not considered to constrain marine microbial activity. Nonetheless, in a model system in which a marine bacterium obtains all of its carbon from co-cultured phytoplankton, bacterial gene expression suggests that at least seven dissolved organic sulfur (DOS) metabolites support bacterial heterotrophy. These labile exometabolites of marine dinoflagellates and diatoms include taurine, N-acetyltaurine, isethionate, choline-O-sulfate, cysteate, 2,3-dihydroxypropane-1-sulfonate (DHPS), and dimethylsulfoniopropionate (DMSP). Leveraging from the compounds identified in this model system, we assessed the role of sulfur metabolites in the ocean carbon cycle by mining the Tara Oceans dataset for diagnostic genes. In the 1.4 million bacterial genome equivalents surveyed, estimates of the frequency of genomes harboring the capability for DOS metabolite utilization ranged broadly, from only 1 out of every 190 genomes (for the C2 sulfonate isethionate) to 1 out of every 5 (for the sulfonium compound DMSP). Bacteria able to participate in DOS transformations are dominated by Alphaproteobacteria in the surface ocean, but by SAR324, Acidimicrobiia, and Gammaproteobacteria at mesopelagic depths, where the capability for utilization occurs in higher frequency than in surface bacteria for more than half the sulfur metabolites. The discovery of an abundant and diverse suite of marine bacteria with the genetic capacity for DOS transformation argues for an important role for sulfur metabolites in the pelagic ocean carbon cycle.
| S-EPMC6776065 | biostudies-literature
Project description:BackgroundThe link between biodiversity and ecosystem processes has firmly been established, but the mechanisms underpinning this relationship are poorly documented. Most studies have focused on terrestrial plant systems where resource use can be difficult to quantify as species rely on a limited number of common resources. Investigating resource use at the bulk level may not always be of sufficient resolution to detect subtle differences in resource use, as species-specific nutritional niches at the biochemical level may also moderate diversity effects on resource use.Methodology/principal findingsHere we use three co-occurring marine benthic echinoderms (Brissopsis lyrifera, Mesothuria intestinalis, Parastichopus tremulus) that feed on the same phytodetrital food source, to determine whether resource partitioning is the principal mechanism underpinning diversity effects on resource use. Specifically we investigate the use of phytodetrital pigments (chlorophylls and carotenoids) because many of these are essential for biological functions, including reproduction. Pigments were identified and quantified using reverse-phase high performance liquid Chromatography (HPLC) and data were analysed using a combination of extended linear regression with generalised least squares (GLS) estimation and standard multivariate techniques. Our analyses reveal no species-specific selectivity for particular algal pigments, confirming that these three species do not partition food resources at the biochemical level. Nevertheless, we demonstrate increased total resource use in diverse treatments as a result of selection effects and the dominance of one species (B. lyrifera).ConclusionOverall, we found no evidence for resource partitioning at the biochemical level, as pigment composition was similar between individuals, which is likely due to plentiful food availability. Reduced intra-specific competition in the species mixture combined with greater adsorption efficiency and differences in feeding behaviour likely explain the dominant use of resources by B. lyrifera.
| S-EPMC2759289 | biostudies-literature
Project description:Essential fatty acids (EFA), which are primarily generated by phytoplankton, limit growth and reproduction in diverse heterotrophs. The biochemical composition of phytoplankton is well-known to be governed both by phylogeny and environmental conditions. Nutrients, light, salinity, and temperature all affect both phytoplankton growth and fatty acid composition. However, the relative importance of taxonomy and environment on algal fatty acid content has yet to be comparatively quantified, thus inhibiting predictions of changes to phytoplankton food quality in response to global environmental change. We compiled 1145 published marine and freshwater phytoplankton fatty acid profiles, consisting of 208 species from six major taxonomic groups, cultured in a wide range of environmental conditions, and used a multivariate distance-based linear model to quantify the total variation explained by each variable. Our results show that taxonomic group accounts for 3-4 times more variation in phytoplankton fatty acids than the most important growth condition variables. The results underscore that environmental conditions clearly affect phytoplankton fatty acid profiles, but also show that conditions account for relatively low variation compared to phylogeny. This suggests that the underlying mechanism determining basal food quality in aquatic habitats is primarily phytoplankton community composition, and allows for prediction of environmental-scale EFA dynamics based on phytoplankton community data. We used the compiled dataset to calculate seasonal dynamics of long-chain EFA (LCEFA; ?C20 ?-3 and ?-6 polyunsaturated fatty acid) concentrations and ?-3:?-6 EFA ratios in Lake Washington using a multi-decadal phytoplankton community time series. These analyses quantify temporal dynamics of algal-derived LCEFA and food quality in a freshwater ecosystem that has undergone large community changes as a result of shifting resource management practices, highlighting diatoms, cryptophytes and dinoflagellates as key sources of LCEFA. Moreover, the analyses indicate that future shifts towards cyanobacteria-dominated communities will result in lower LCEFA content in aquatic ecosystems.
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