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Autotrophs do not depend on other organism for their food. They are the primary producer and are placed first in the food chain. Heterotrophs that depend on autotrophs and other heterotrophs for their energy level are placed next on the food chain.

Stoichiometric nutrient ratios are the consequence of myriad interacting processes, both biotic and abiotic. Theoretical explanations for autotroph stoichiometry have focused on species' nutrient requirements but have not addressed the role of nutrient availability in determining autotroph stoichiometry. Remineralization of organic N and P supplies a significant fraction of inorganic N and P to autotrophs, making nutrient recycling a potentially important process influencing autotroph stoichiometry. To quantitatively investigate the relationship between available N and P, autotroph N:P, and nutrient recycling, we analyze a stoichiometrically explicit model of autotroph growth, incorporating Michaelis-Menten-Monod nutrient uptake kinetics, Droop growth, and Liebig's law of the minimum. If autotroph growth is limited by a single nutrient, increased recycling of the limiting nutrient pushes autotrophs toward colimitation and alters both autotroph and environmental stoichiometry. We derive a steady state relationship between input stoichiometry, autotroph N:P, and the stoichiometry of organic losses that allows us to estimate the relative recycling of N to P within an ecosystem. We then estimate relative N and P recycling for a marine, an aquatic, and two terrestrial ecosystems. Preferential P recycling, in conjunction with greater relative P retention at the organismal and ecosystem levels, presents a strong case for the importance of P to biomass production across ecosystems.

CBBp+RuBisCO (black line) and CBBp+RuBisCO (purple line) were cultivated under chemoorganoautotrophic conditions and the mean of at least three biological replicates (independent transformations) with single values (black and purple signs) is shown.

Citation: Hunt KA, Jennings RM, Inskeep WP, Carlson RP (2018) Multiscale analysis of autotroph-heterotroph interactions in a high-temperature microbial community. PLoS Comput Biol 14(9): e1006431.

Carbon dioxide fixation by autotrophs in the community contributes 42 to 99% of the total microbial biomass carbon in Fe(III)-oxide mats from Beowulf and OSP hot springs; the remaining carbon originates from exogenous sources that are produced independent of system electron donor and acceptor requirements [17]. Carbon dioxide fixation has been demonstrated in M. yellowstonensis, which is one of the primary autotrophs in the oxic zones of the Fe(III)-oxide mats [17,19]. Metagenome analysis has established Geoarchaeum str. OSPB as a primary aerobic heterotroph, which comprises 30 to 50% of the total microbial community in the oxic zones of Fe(III)-oxide mats found at OSP [7,12]. Chemolithoautotrophic metabolism and the subsequent transfer of nutrients and energy to heterotrophs (e.g. Geoarchaeum str. OSPB) is hypothesized to drive major autotroph-heterotroph interactions along with competition for the primary terminal electron acceptor, oxygen. Sulfolobales viruses are highly represented in the metagenome sequence of these Fe(III)-oxide mats [10], which suggests that viral predation of M. yellowstonensis and other Sulfolobales populations contributes to the turnover of autotrophic biomass and creates reduced carbon sources for heterotrophs.

A primary goal in environmental microbiology is to understand and predict microbial behavior in communities, where interactions among different populations lead to emergent properties, such as enhanced productivity, stability, and robustness [29]. Consequently, the objectives of this study were to 1) construct metabolic network models for major autotroph and heterotroph populations present in oxic zones of high-temperature Fe(III)-oxide mats using metagenome sequence assemblies from representative sites; 2) analyze the use of electron donors and acceptors for the production of biomass and cellular energy under different nutrient limitations; 3) integrate individual population models to examine possible autotroph-heterotroph interactions that may be fundamental to the ecology of microbial communities (e.g. relative population abundances and oxygen competition); and 4) perform a sensitivity analysis based on parameters measured in situ to determine model limitations and identify future priorities for field measurements. The approach used here integrates data from the nanoscale of electron transport to microscale oxygen depth-profiles to hot spring-scale measurements of biotic Fe(III)-oxide deposition. Novel insights and governing principles of community structure and function were established through the integration of metagenome-enabled in silico approaches and in situ measurements.

Genomic data were used to construct in silico representations of the electron transport network responsible for the oxidation of Fe(II) and sulfur species and the reduction of oxygen in M. yellowstonensis str. MK1 (Fig 1). Genomic and physiological evidence indicated that this chemolithoautotroph oxidizes Fe(II) using proteins encoded by the fox operon, which are also found in other Sulfolobales [16]. M. yellowstonensis can also oxidize a variety of sulfur species, including sulfide, elemental sulfur, sulfite, and thiosulfate, to reduce the quinone pool to quinol [16]. Electrons in the quinol pool can drive cellular energy production via oxidative phosphorylation through the reduction of oxygen using a high affinity heme copper oxidase. Alternatively, electrons in the quinol pool can reduce NAD+, enter central carbon metabolism, and be used to reduce inorganic carbon via the 3-hydroxypropionate / 4-hydroxybutyrate (3-HP / 4-HB) pathway [17]. These electron transport pathways are hypothesized to provide the majority of energy to the studied microbial communities. The modeled central carbon metabolism of M. yellowstonensis included the tricarboxylic acid cycle, gluconeogenesis, the pentose phosphate pathway via ribulose monophosphate [30], and the mevalonate pathway [31].

A) Moles of oxygen and electron donor required to produce one Cmole of M. yellowstonensis biomass for all biomass producing elementary flux modes, note the log scales. Clusters of electron donors, which include Fe(II), sulfide, sulfur, sulfite, and thiosulfate, are circled by dashed lines. B) Moles of oxygen and autotroph biomass required to produce one Cmole of Geoarchaeum str. OSPB biomass. Optimizations for carbon- and oxygen-limited scenarios are marked by points A and B, respectively. C) Relative oxygen consumption plotted as a function of biomass production for autotroph, M. yellowstonensis, utilizing Fe(II) or elemental sulfur, and for heterotroph, Geoarchaeum str. OSPB, utilizing autotroph biomass generated from Fe(II) oxidation or exogenous sources of reduced organic carbon (i.e. landscape carbon).

Genomic analysis of Geoarchaeum str. OSPB indicated that this organism is an organoheterotroph with the metabolic potential to utilize a wide variety of reduced carbon species, including biomass macromolecules (i.e. lipids, peptides, polysaccharides, and nucleic acids; see the supplemental material or [34] for a description of reactions involved). Details of Geoarchaeum biomass production from components of lysed Metallosphaera cells were elucidated in a prior report [34]. Briefly, the production of heterotroph biomass based on the consumption of autotroph biomass as a carbon source was evaluated with respect to the Cmoles of carbon substrate or moles of oxygen required to produce a Cmole of biomass (Table B in S13 File). The production of a Cmole of Geoarchaeum str. OSPB biomass required 2.4 Cmoles of autotroph biomass to supply the cellular energy and structural components for growth under carbon-limited conditions (Fig 2B, point A). Production of a Cmole of Geoarchaeum str. OSPB biomass under oxygen-limited conditions requires 3.8 Cmoles of autotroph biomass (Fig 2B, point B).

Different scenarios were used to evaluate heterotroph growth in this system: organic carbon was either made available, opportunistically, as a result of viral predation and subsequent lysis of the autotrophic cells, modeled as free monomer pools, or organic carbon was supplied as the result of a biological strategy where metabolites were excreted from the autotroph. Alternatively, organic carbon was provided from the surrounding landscape (hereafter called landscape carbon) which allowed for heterotrophic growth independent of the examined autotroph. The landscape carbon was modeled to have the same macromolecular composition as autotroph biomass for simplicity (supplemental material). The landscape carbon was produced from electron donors and acceptors external to the system boundaries and therefore did not contribute to oxygen consumption in the mat. Heterotroph growth on landscape carbon required 1.6 moles oxygen per Cmole of biomass produced, which is 54 and 96% less than the oxygen required to support the production of autotroph biomass from either elemental sulfur or Fe(II), respectively (Fig 2C, Table B in S13 File). The lower oxygen requirement for organoheterotrophic growth was due to utilization of reduced carbon substrates as both electron donors and anabolic precursors. By comparison, autotrophic metabolism required substantially more energy to reduce carbon dioxide, which resulted in high oxygen requirements, especially when Fe(II) was the primary electron donor. Consequently, the oxygen requirements to produce heterotroph biomass increased sharply when community-level interactions were included. For example, Geoarchaeum str. OSPB requires 2.4 Cmoles of autotroph biomass to produce a Cmole of heterotroph biomass under carbon-limited conditions (Fig 2B, Table B in S13 File). The total, aggregate oxygen requirement to produce heterotroph biomass from the biomass of an Fe(II) oxidizing autotroph included both the oxygen requirements of the heterotroph and the oxygen requirements to produce the autotroph biomass consumed, which resulted in 93 moles of oxygen being consumed per Cmole heterotroph biomass (Fig 2C). 59ce067264

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