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  1. Abstract

    Epithemia spp. diatoms contain obligate, nitrogen-fixing endosymbionts, or diazoplasts, derived from cyanobacteria. These algae are a rare example of photosynthetic eukaryotes that have successfully coupled oxygenic photosynthesis with oxygen-sensitive nitrogenase activity. Here, we report a newly-isolated species, E. clementina, as a model to investigate endosymbiotic acquisition of nitrogen fixation. We demonstrate that the diazoplast, which has lost photosynthesis, provides fixed nitrogen to the diatom host in exchange for fixed carbon. To identify the metabolic changes associated with this endosymbiotic specialization, we compared the Epithemia diazoplast with its close, free-living cyanobacterial relative, Crocosphaera subtropica. Unlike C. subtropica, in which nitrogenase activity is temporally separated from photosynthesis, we show that nitrogenase activity in the diazoplast is continuous through the day (concurrent with host photosynthesis) and night. Host and diazoplast metabolism are tightly coupled to support nitrogenase activity: Inhibition of photosynthesis abolishes daytime nitrogenase activity, while nighttime nitrogenase activity no longer requires cyanobacterial glycogen storage pathways. Instead, import of host-derived carbohydrates supports nitrogenase activity throughout the day-night cycle. Carbohydrate metabolism is streamlined in the diazoplast compared to C. subtropica with retention of the oxidative pentose phosphate pathway and oxidative phosphorylation. Similar to heterocysts, these pathways may be optimized to support nitrogenase activity, providing reducing equivalents and ATP and consuming oxygen. Our results demonstrate that the diazoplast is specialized for endosymbiotic nitrogen fixation. Altogether, we establish a new model for studying endosymbiosis, perform a functional characterization of this diazotroph endosymbiosis, and identify metabolic adaptations for endosymbiotic acquisition of a critical biological function.

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  2. Abstract

    When leaves fall in rivers, microbial decomposition commences within hours. Microbial assemblages comprising hundreds of species of fungi and bacteria can vary with stream conditions, leaf litter species, and decomposition stage. In terrestrial ecosystems, fungi and bacteria that enter soils with dead leaves often play prominent roles in decomposition, but their role in aquatic decomposition is less known. Here, we test whether fungi and bacteria that enter streams on senesced leaves are growing during decomposition and compare their abundances and growth to bacteria and fungi that colonize leaves in the water. We employ quantitative stable isotope probing to identify growing microbes across four leaf litter species and two decomposition times. We find that most of the growing fungal species on decomposing leaves enter the water with the leaf, whereas most growing bacteria colonize from the water column. Results indicate that the majority of bacteria found on litter are growing, whereas the majority of fungi are dormant. Both bacterial and fungal assemblages differed with leaf type on the dried leaves and throughout decomposition. This research demonstrates the importance of fungal species that enter with the leaf on aquatic decomposition and the prominence of bacteria that colonize decomposing leaves in the water.

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  3. As terrestrial leaf litter decomposes in rivers, its constituent elements follow multiple pathways. Carbon leached as dissolved organic matter can be quickly taken up by microbes, then respired before it can be transferred to the macroscopic food web. Alternatively, this detrital carbon can be ingested and assimilated by aquatic invertebrates, so it is retained longer in the stream and transferred to higher trophic levels. Microbial growth on litter can affect invertebrates through three pathways, which are not mutually exclusive. First, microbes can facilitate invertebrate feeding, improving food quality by conditioning leaves and making them more palatable for invertebrates. Second, microbes can be prey for invertebrates. Third, microbes can compete with invertebrates for resources bound within litter and may produce compounds that retard carbon and nitrogen fluxes to invertebrates. As litter is broken down into smaller particles, there are many opportunities for its elements to reenter the stream food web. Here, I describe a conceptual framework for evaluating how traits of leaf litter will affect its fate in food webs and ecosystems that is useful for predicting how global change will alter carbon fluxes into and out of streams. 
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  4. Lemon, Katherine P. (Ed.)
    ABSTRACT Predation structures food webs, influences energy flow, and alters rates and pathways of nutrient cycling through ecosystems, effects that are well documented for macroscopic predators. In the microbial world, predatory bacteria are common, yet little is known about their rates of growth and roles in energy flows through microbial food webs, in part because these are difficult to quantify. Here, we show that growth and carbon uptake were higher in predatory bacteria compared to nonpredatory bacteria, a finding across 15 sites, synthesizing 82 experiments and over 100,000 taxon-specific measurements of element flow into newly synthesized bacterial DNA. Obligate predatory bacteria grew 36% faster and assimilated carbon at rates 211% higher than nonpredatory bacteria. These differences were less pronounced for facultative predators (6% higher growth rates, 17% higher carbon assimilation rates), though high growth and carbon assimilation rates were observed for some facultative predators, such as members of the genera Lysobacter and Cytophaga , both capable of gliding motility and wolf-pack hunting behavior. Added carbon substrates disproportionately stimulated growth of obligate predators, with responses 63% higher than those of nonpredators for the Bdellovibrionales and 81% higher for the Vampirovibrionales , whereas responses of facultative predators to substrate addition were no different from those of nonpredators. This finding supports the ecological theory that higher productivity increases predator control of lower trophic levels. These findings also indicate that the functional significance of bacterial predators increases with energy flow and that predatory bacteria influence element flow through microbial food webs. IMPORTANCE The word “predator” may conjure images of leopards killing and eating impala on the African savannah or of great white sharks attacking elephant seals off the coast of California. But microorganisms are also predators, including bacteria that kill and eat other bacteria. While predatory bacteria have been found in many environments, it has been challenging to document their importance in nature. This study quantified the growth of predatory and nonpredatory bacteria in soils (and one stream) by tracking isotopically labeled substrates into newly synthesized DNA. Predatory bacteria were more active than nonpredators, and obligate predators, such as Bdellovibrionales and Vampirovibrionales , increased in growth rate in response to added substrates at the base of the food chain, strong evidence of trophic control. This work provides quantitative measures of predator activity and suggests that predatory bacteria—along with protists, nematodes, and phages—are active and important in microbial food webs. 
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