Cooperative Metabolism in a Three-Partner Insect-Bacterial Symbiosis Revealed by Metabolic Modeling

ABSTRACT An important factor determining the impact of microbial symbionts on their animal hosts is the balance between the cost of nutrients consumed by the symbionts and the benefit of nutrients released back to the host, but the quantitative significance of nutrient exchange in symbioses involving multiple microbial partners has rarely been addressed. In this study on the association between two intracellular bacterial symbionts, “Candidatus Portiera aleyrodidarum” and “Candidatus Hamiltonella defensa,” and their animal host, the whitefly Bemisia tabaci, we apply metabolic modeling to investigate host-symbiont nutrient exchange. Our in silico analysis revealed that >60% of the essential amino acids and related metabolites synthesized by “Candidatus Portiera aleyrodidarum” are utilized by the host, including a substantial contribution of nitrogen recycled from host nitrogenous waste, and that these interactions are required for host growth. In contrast, “Candidatus Hamiltonella defensa” retains most or all of the essential amino acids and B vitamins that it is capable of synthesizing. Furthermore, “Candidatus Hamiltonella defensa” suppresses host growth in silico by competition with “Candidatus Portiera aleyrodidarum” for multiple host nutrients, by suppressing “Candidatus Portiera aleyrodidarum” growth and metabolic function, and also by consumption of host nutrients that would otherwise be allocated to host growth. The interpretation from these modeling outputs that “Candidatus Hamiltonella defensa” is a nutritional parasite could not be inferred reliably from gene content alone but requires consideration of constraints imposed by the structure of the metabolic network. Furthermore, these quantitative models offer precise predictions for future experimental study and the opportunity to compare the functional organization of metabolic networks in different symbioses. IMPORTANCE The metabolic functions of unculturable intracellular bacteria with much reduced genomes are traditionally inferred from gene content without consideration of how the structure of the metabolic network may influence flux through metabolic reactions. The three-compartment model of metabolic flux between two bacterial symbionts and their insect host constructed in this study revealed that one symbiont is structured to overproduce essential amino acids for the benefit of the host, but the essential amino acid production in the second symbiont is quantitatively constrained by the structure of its network, rendering it “selfish” with respect to these nutrients. This study demonstrates the importance of quantitative flux data for elucidation of the metabolic function of symbionts. The in silico methodology can be applied to other symbioses with intracellular bacteria.

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Nutritional quality evaluation of Whitemouth croaker (Micropogonias furnieri) protein isolate

Nutrition & Food Science ◽

10.1108/nfs-06-2013-0070 ◽

2014 ◽

Vol 44 (2) ◽

pp. 134-143

Author(s):

William Renzo Cortez-Vega ◽

Irene Rodrigues Freitas ◽

Sandriane Pizato ◽

Carlos Prentice

Keyword(s):

Amino Acids ◽

Amino Acid ◽

Nutritional Quality ◽

Troponin I ◽

Essential Amino Acids ◽

Protein Isolate ◽

Content Type ◽

Sds Page ◽

Apparent Bioavailability

Purpose – The purpose of this study was to isolate Whitemouth croaker protein by alkaline solubilization process and evaluate their nutritional quality to evaluate the bioavailability of essential amino acids. Design/methodology/approach – The proximate composition, essential amino acid composition, in vitro digestibility, apparent bioavailability, chemical score of amino acids and SDS-PAGE were determined for the isolated croaker proteins. Findings – The isolated protein showed a high level of protein 92.21 percent and low amount of lipids 0.57 percent. The protein is rich in lysine and leucine, 108.73 and 96.75 mg/g protein, respectively. The protein isolate had high digestibility, 94.32 percent, which indicates proper utilization of this protein source, while the tryptophan had lower bioavailability (12.58 mg amino acid/mg protein). The high chemical scores were found for the amino acids lysine, methionine+cysteine (6.79 and 5.14). SDS-PAGE of proteins extracted showed appearance of the heavy chain of myosin (220 kDa), actin (50 kDa) and other fractions, with molecular weight between 20 and 50 kDa, such as troponin I, C and T. Originality/value – The products obtained from croaker muscle can be incorporated as a high value supplements in human diets. The isolated protein exhibited a high content of essential amino acids and digestibility, indicating that the protein has a high nutritional quality.

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Genome analyses of a placozoan rickettsial endosymbiont show a combination of mutualistic and parasitic traits

Scientific Reports ◽

10.1038/s41598-019-54037-w ◽

2019 ◽

Vol 9 (1) ◽

Cited By ~ 3

Author(s):

Kai Kamm ◽

Hans-Jürgen Osigus ◽

Peter F. Stadler ◽

Rob DeSalle ◽

Bernd Schierwater

Keyword(s):

Amino Acids ◽

Environmental Conditions ◽

Metabolic Pathways ◽

Essential Amino Acids ◽

Intracellular Bacteria ◽

The Novel ◽

Symbiotic Relationships ◽

Genome Analyses ◽

Growth And Reproduction

AbstractSymbiotic relationships between eukaryotic hosts and bacteria range from parasitism to mutualism and may deeply influence both partners’ fitness. The presence of intracellular bacteria in the metazoan phylum Placozoa has been reported several times, but without any knowledge about the nature of this relationship and possible implications for the placozoan holobiont. This information may be of crucial significance since little is known about placozoan ecology and how different species adapt to different environmental conditions, despite being almost invariable at the morphological level. We here report on the novel genome of the rickettsial endosymbiont of Trichoplax sp. H2 (strain “Panama”). The combination of eliminated and retained metabolic pathways of the bacterium indicates a potential for a mutualistic as well as for a parasitic relationship, whose outcome could depend on the environmental context. In particular we show that the endosymbiont is dependent on the host for growth and reproduction and that the latter could benefit from a supply with essential amino acids and important cofactors. These findings call for further studies to clarify the actual benefit for the placozoan host and to investigate a possible role of the endosymbiont for ecological separation between placozoan species.

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Interrogation of the Perturbed Gut Microbiota in Gouty Arthritis Patients Through in silico Metabolic Modeling

10.1101/2020.09.02.20187013 ◽

2020 ◽

Author(s):

Michael A. Henson

Keyword(s):

Amino Acids ◽

Uric Acid ◽

Amino Acid ◽

Gut Microbiota ◽

In Silico ◽

Gouty Arthritis ◽

Metabolic Modeling ◽

Patient Specific ◽

Surprising Result ◽

Sulfur Containing

Recent studies have shown perturbed gut microbiota associated with gouty arthritis, a metabolic disease in which an imbalance between uric acid production and excretion leads to the deposition of uric acid crystals in joints. To mechanistically investigate altered microbiota metabolism in gout disease, 16S rRNA gene amplicon sequence data from stool samples of gout patients and healthy controls were computationally analyzed through bacterial community metabolic modeling. Patient-specific models were used to cluster samples according to their metabolic capabilities and to generate statistically significant partitioning of the samples into a Bacteroides-dominated, high gout cluster and a Faecalibacterium-elevated, low gout cluster. The high gout cluster samples were predicted to allow elevated synthesis of the amino acids D-alanine and L-alanine and byproducts of branched-chain amino acid catabolism, while the low gout cluster samples allowed higher production of butyrate, the sulfur-containing amino acids L-cysteine and L-methionine and the L-cysteine catabolic product H2S. The models predicted an important role for metabolite crossfeeding, including the exchange of acetate, D-lactate and succinate from Bacteroides to Faecalibacterium to allow higher butyrate production differences than would be expected based on taxa abundances in the two clusters. The surprising result that the high gout cluster could underproduce H2S despite having a higher abundance of H2S-synthesizing bacteria was rationalized by reduced L-cysteine production from Faecalibacterium in this cluster. Model predictions were not substantially altered by constraining uptake rates with different in silico diets, suggesting that sulfur-containing amino acid metabolism generally and H2S more specifically could be novel gout disease markers.

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Quality of gluten-free cookies made with rice flour of different levels of amylose and cowpea beans

British Food Journal ◽

10.1108/bfj-09-2020-0860 ◽

2020 ◽

Vol ahead-of-print (ahead-of-print) ◽

Author(s):

Estefania Julia Dierings de Souza ◽

Aline Machado Pereira ◽

Mauro Fontana ◽

Nathan Levien Vanier ◽

Marcia Arocha Gularte

Keyword(s):

Amino Acids ◽

Protein Digestibility ◽

Rice Flour ◽

Essential Amino Acids ◽

Gluten Free ◽

Content Type ◽

High Amylose ◽

Different Levels

PurposeThe objective of this study was to evaluate the effects of rice flour obtained from rice grains with different levels of amylose on technological, nutritional and sensory properties of cookies made with a blend of rice and cowpea flour.Design/methodology/approachThe cookies preparation was set at a ratio of rice flour and cowpea beans 70:30. The studied formulations were: LA: low amylose rice flour; MA: medium-amylose rice flour; HA: high amylose rice flour. The quality of the obtained cookies was analyzed for proximate composition, in vitro protein digestibility, thickness, diameter, dispersion factor, texture, color, amino acid profile and sensory properties.FindingsProximate composition and in vitro protein digestibility showed no differences between the three studied formulations. The medium and low amylose rice flour cookies showed the lowest hardness values. The combination of rice and beans allowed a good balance of essential amino acids. The cookies formulated with high amylose rice flour presented lighter coloration, low hardness and greater sensory preference.Originality/valueRice and cowpea flours are an alternative source for the preparation of gluten-free bakery products, such as cookies. The high amylose content of rice flour has less negative interference in the texture characteristics of the cookies. The combination of rice and beans flour provides a balance of essential amino acids.

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Nutritional quality evaluation of surimi and kamaboko obtained from mechanically separated chicken meat

Nutrition & Food Science ◽

10.1108/nfs-11-2013-0140 ◽

2014 ◽

Vol 44 (6) ◽

pp. 483-491 ◽

Cited By ~ 5

Author(s):

William Renzo Cortez-Vega ◽

Sandriane Pizato ◽

Carlos Prentice

Keyword(s):

Amino Acids ◽

Amino Acid ◽

Nutritional Quality ◽

Essential Amino Acids ◽

Chicken Meat ◽

Content Type ◽

Minimum Requirement ◽

Limiting Amino Acid ◽

Apparent Bioavailability

Purpose – The purpose of this paper was to determine the nutritional quality of the surimi and kamaboko obtained from mechanically separated chicken meat and evaluate the bioavailability of essential amino acids found in these products. Design/methodology/approach – The mechanically separated chicken meat (MSCM) was characterized by the proximate composition, and the surimi and kamaboko were characterized by in vitro digestibility, determination of chemical score of amino acids and apparent bioavailability. Findings – The MSCM contains 68.1 ± 0.5, 12.9 ± 0.24, 18.5 ± 0.28 and 0.6 ± 0.06 per cent moisture, protein, lipids and ash, respectively. The moisture of the MSCM (surimi) was 80.45 ± 0.15 per cent, and the protein was 10.04 ± 0.21 per cent. The highest digestibility was found for the kamaboko (92.27 per cent) which was heat-treated and the lowest was for surimi (90.82 per cent). Histidine is a limiting amino acid. In this study, the surimi showed 84.69 per cent and the kamaboko presented 81.31 per cent of the minimum requirement for adults. In relation to the apparent bioavailability, there was a decrease of surimi to kamaboko of 2.52 per cent of the limiting amino acid histidine. The surimi and the kamaboko presented 76.94 and 75 per cent of the minimum requirement for adults, respectively. Originality/value – The application of the surimi technology in the production of a surimi-like material from mechanically deboned chicken meat provides a new approach toward increasing its value and utilization, e.g. for the development of meat-based products and analogs, as alternative protein sources, the surimi and the kamaboko exhibited a high content of essential amino acids, indicating that the protein has a relatively high nutritional quality.

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Proteomic and Transcriptomic Changes in Hibernating Grizzly Bears Reveal Metabolic and Signaling Pathways that Protect against Muscle Atrophy

Scientific Reports ◽

10.1038/s41598-019-56007-8 ◽

2019 ◽

Vol 9 (1) ◽

Cited By ~ 5

Author(s):

D. A. Mugahid ◽

T. G. Sengul ◽

X. You ◽

Y. Wang ◽

L. Steil ◽

...

Keyword(s):

Gene Expression ◽

Amino Acids ◽

Muscle Atrophy ◽

Physiological Response ◽

Metabolic Modeling ◽

Essential Amino Acids ◽

Grizzly Bears ◽

Grizzly Bear ◽

C Elegans ◽

Transcriptomic Changes

AbstractMuscle atrophy is a physiological response to disuse and malnutrition, but hibernating bears are largely resistant to this phenomenon. Unlike other mammals, they efficiently reabsorb amino acids from urine, periodically activate muscle contraction, and their adipocytes differentially responds to insulin. The contribution of myocytes to the reduced atrophy remains largely unknown. Here we show how metabolism and atrophy signaling are regulated in skeletal muscle of hibernating grizzly bear. Metabolic modeling of proteomic changes suggests an autonomous increase of non-essential amino acids (NEAA) in muscle and treatment of differentiated myoblasts with NEAA is sufficient to induce hypertrophy. Our comparison of gene expression in hibernation versus muscle atrophy identified several genes differentially regulated during hibernation, including Pdk4 and Serpinf1. Their trophic effects extend to myoblasts from non-hibernating species (including C. elegans), as documented by a knockdown approach. Together, these changes reflect evolutionary favored adaptations that, once translated to the clinics, could help improve atrophy treatment.

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Essential amino acids profile of differentially processed soy products and their efficiency in meeting daily requirement

Nutrition & Food Science ◽

10.1108/nfs-07-2015-0082 ◽

2016 ◽

Vol 46 (2) ◽

pp. 237-245 ◽

Cited By ~ 4

Author(s):

Vineet Kumar ◽

Anita Rani ◽

Lulua Hussain

Keyword(s):

Amino Acids ◽

High Performance ◽

Aromatic Amino Acids ◽

Essential Amino Acids ◽

Soy Flour ◽

Soy Milk ◽

Content Type ◽

Alternate Source ◽

Amino Acids Profile ◽

Spray Dried

Purpose – In the backdrop of declining per capita availability of pulses, soybean is the alternate source to address protein deficiency in India. The study aims to assess the efficiency of soy products available in the market for meeting the daily requirement of essential amino acids (EAAs). Design/methodology/approach – Extruded soy products, namely, soy nuggets, granules, soy flour manufactured from sprouts, spray-dried soy milk variants, ready-to-drink (RTD) soy beverage and silken tofu, were analysed for EAAs by high-performance liquid chromatography. In addition, efficiency of these products in terms of meeting the daily requirement of EAAs for an adult weighing 70 kg through a single serving (equivalent to 6 g protein) was also computed. Findings – Leucine was the most concentrated EAA in all the soy products, except in variants of soy milk. Total essential amino acids’ (TEAAs) content in soy flour was significantly higher compared to soy nuggets and granules. Spray-dried plain soymilk exhibited a significantly higher level of TEAAs content compared to flavoured variant and RTD soy beverage. Among all the products, silken tofu exhibited the highest concentration of TEAAs. RTD soy beverage was the most efficient product for meeting the daily requirement of isoleucine and valine, soy flour for aromatic amino acids and silken tofu for lysine and leucine. Originality/value – This work pertains to the determination of EAAs of commercial soy products and assesses their efficiency in terms of meeting the daily requirement of EAAs. This type of technical evaluation of soy products has not been conducted earlier.

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The Cost of Metabolic Interactions in Symbioses between Insects and Bacteria with Reduced Genomes

mBio ◽

10.1128/mbio.01433-18 ◽

2018 ◽

Vol 9 (5) ◽

Cited By ~ 14

Author(s):

Nana Y. D. Ankrah ◽

Bessem Chouaia ◽

Angela E. Douglas

Keyword(s):

Metabolic Cost ◽

Essential Amino Acids ◽

Genome Reduction ◽

Bacterial Symbionts ◽

Relaxed Selection ◽

Content Type ◽

Genome Data ◽

Metabolic Functions ◽

Metabolite Exchange ◽

Metabolic Models

ABSTRACTVarious intracellular bacterial symbionts that provide their host with essential nutrients have much-reduced genomes, attributed largely to genomic decay and relaxed selection. To obtain quantitative estimates of the metabolic function of these bacteria, we reconstructed genome- and transcriptome-informed metabolic models of three xylem-feeding insects that bear two bacterial symbionts with complementary metabolic functions: a primary symbiont,Sulcia, that has codiversified with the insects, and a coprimary symbiont of distinct taxonomic origin and with different degrees of genome reduction in each insect species (Hodgkiniain a cicada,Baumanniain a sharpshooter, andSodalisin a spittlebug). Our simulations reveal extensive bidirectional flux of multiple metabolites between each symbiont and the host, but near-complete metabolic segregation (i.e., near absence of metabolic cross-feeding) between the two symbionts, a likely mode of host control over symbiont metabolism. Genome reduction of the symbionts is associated with an increased number of host metabolic inputs to the symbiont and also reduced metabolic cost to the host. In particular,SulciaandHodgkiniawith genomes of ≤0.3 Mb are calculated to recycle ∼30 to 80% of host-derived nitrogen to essential amino acids returned to the host, whileBaumanniaandSodaliswith genomes of ≥0.6 Mb recycle 10 to 15% of host nitrogen. We hypothesize that genome reduction of symbionts may be driven by selection for increased host control and reduced host costs, as well as by the stochastic process of genomic decay and relaxed selection.IMPORTANCECurrent understanding of many animal-microbial symbioses involving unculturable bacterial symbionts with much-reduced genomes derives almost entirely from nonquantitative inferences from genome data. To overcome this limitation, we reconstructed multipartner metabolic models that quantify both the metabolic fluxes within and between three xylem-feeding insects and their bacterial symbionts. This revealed near-complete metabolic segregation between cooccurring bacterial symbionts, despite extensive metabolite exchange between each symbiont and the host, suggestive of strict host controls over the metabolism of its symbionts. We extended the model analysis to investigate metabolic costs. The positive relationship between symbiont genome size and the metabolic cost incurred by the host points to fitness benefits to the host of bearing symbionts with small genomes. The multicompartment metabolic models developed here can be applied to other symbioses that are not readily tractable to experimental approaches.

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Microbiomes of Blood-Feeding Arthropods: Genes Coding for Essential Nutrients and Relation to Vector Fitness and Pathogenic Infections. A Review

Microorganisms ◽

10.3390/microorganisms9122433 ◽

2021 ◽

Vol 9 (12) ◽

pp. 2433

Author(s):

Daniel E. Sonenshine ◽

Philip E. Stewart

Keyword(s):

Normal Development ◽

Gene Families ◽

Enteric Bacteria ◽

Essential Amino Acids ◽

Blood Feeding ◽

Bacterial Symbionts ◽

Essential Nutrients ◽

Blood Sucking ◽

Host Growth ◽

Vector Borne

Background: Blood-feeding arthropods support a diverse array of symbiotic microbes, some of which facilitate host growth and development whereas others are detrimental to vector-borne pathogens. We found a common core constituency among the microbiota of 16 different arthropod blood-sucking disease vectors, including Bacillaceae, Rickettsiaceae, Anaplasmataceae, Sphingomonadaceae, Enterobacteriaceae, Pseudomonadaceae, Moraxellaceae and Staphylococcaceae. By comparing 21 genomes of common bacterial symbionts in blood-feeding vectors versus non-blooding insects, we found that certain enteric bacteria benefit their hosts by upregulating numerous genes coding for essential nutrients. Bacteria of blood-sucking vectors expressed significantly more genes (p < 0.001) coding for these essential nutrients than those of non-blooding insects. Moreover, compared to endosymbionts, the genomes of enteric bacteria also contained significantly more genes (p < 0.001) that code for the synthesis of essential amino acids and proteins that detoxify reactive oxygen species. In contrast, microbes in non-blood-feeding insects expressed few gene families coding for these nutrient categories. We also discuss specific midgut bacteria essential for the normal development of pathogens (e.g., Leishmania) versus others that were detrimental (e.g., bacterial toxins in mosquitoes lethal to Plasmodium spp.).

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Effect of migratory locust (Locusta migratoria) powder incorporation on nutritional and sensorial properties of wheat flour bread

British Food Journal ◽

10.1108/bfj-11-2020-1052 ◽

2021 ◽

Vol ahead-of-print (ahead-of-print) ◽

Author(s):

Sami A. Althwab ◽

Raghad M. Alhomaid ◽

Rehab F. M. Ali ◽

Ayman Mohammed El-Anany ◽

Hassan M. Mousa

Keyword(s):

Amino Acids ◽

Binary Mixture ◽

Wheat Flour ◽

Functional Properties ◽

Locusta Migratoria ◽

Essential Amino Acids ◽

Mineral Elements ◽

Absorption Capacity ◽

Migratory Locust ◽

Content Type

PurposeThe effects of incorporation of Locusta migratoria (LM) powder at different levels (0, 1, 2, 3, 4 and 5%) on nutritional, qualitative and sensory properties of baked breads were investigated.Design/methodology/approachChemical composition, mineral elements and functional properties of wheat flour, LM powder and their binary mixture systems were determined. The breads were assayed for proximate composition, minerals, amino acids profile, physical characteristics and sensorial properties.FindingsLM powder have relatively high levels of protein (51.97% db), fat (23.15% db) and fibers (13.76% db). LM powder presented significantly (p ≤ 0.05) greater water absorption capacity (WAC), oil absorption capacity(OAC), emulsion activity (EA) and foam capacity (FC) as compared to wheat flour. Blending wheat flour with various levels of LM powder significantly (p ≤ 0.05) improved the functional properties of binary mixture systems. Protein, fat, fiber and ash contents of bread samples significantly increased with the addition of LM powder. No significant differences (p ≤ 0.05) were recorded in specific volume between control breads and those breads containing LM powder up to 2%. Breads fortified with LM powder contained higher values of essential amino acids than the limits of FAO/WHO pattern, with exception of lysine. Sensory evaluation results showed that bread samples with the addition of LM powder at levels 1–4% had high overall acceptability.Research limitations/implicationsLimitations of our study are the lack of approved and professional programs about management, collection, harvesting, processing, marketing and consumption of edible insects; therefore, these results should be generalized implications for industry. This present study, therefore, provides useful data to support public health nutrition aimed at improving the nutritional health of populations through the promotion of bakery products enriched with LM powder.Practical implicationsThe main findings of this study indicated that the addition of 1–4% of LM powder into wheat flour enhanced sensory and nutritional properties of produced breads.Originality/valueIt is concluded that the addition of LM powder improves the nutritional and sensorial properties of the produced bread when the wheat flour is substituted with 1–4% of LM powder.

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