Uric acid metabolism by symbiotic bacteria from the fat body of Periplaneta americana

Donnellan, John F.; Kilby, B. A.

doi:10.1016/0010-406x(67)90184-3

Cited by 39 publications

(9 citation statements)

References 20 publications

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“…However, our results show that the endosymbiont genome does not code for any activity related to either the synthesis or the catabolism of urates. Therefore, and contrary to early reports based on putative cultured endosymbiotic bacteria [29], Blattabacterium strain Bge cannot participate in the metabolism of this nitrogen compound directly. Since uricase activity has been detected in the fat body of the cockroach [28],[34],[35], the host could contribute with uric-derived metabolites to the nitrogen economy of the endosymbiont which, in turn, would produce ammonia and carbon dioxide as final catabolic products.…”

Section: Resultscontrasting

confidence: 78%

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Evolutionary Convergence and Nitrogen Metabolism in Blattabacterium strain Bge, Primary Endosymbiont of the Cockroach Blattella germanica

et al. 2009

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Bacterial endosymbionts of insects play a central role in upgrading the diet of their hosts. In certain cases, such as aphids and tsetse flies, endosymbionts complement the metabolic capacity of hosts living on nutrient-deficient diets, while the bacteria harbored by omnivorous carpenter ants are involved in nitrogen recycling. In this study, we describe the genome sequence and inferred metabolism of Blattabacterium strain Bge, the primary Flavobacteria endosymbiont of the omnivorous German cockroach Blattella germanica. Through comparative genomics with other insect endosymbionts and free-living Flavobacteria we reveal that Blattabacterium strain Bge shares the same distribution of functional gene categories only with Blochmannia strains, the primary Gamma-Proteobacteria endosymbiont of carpenter ants. This is a remarkable example of evolutionary convergence during the symbiotic process, involving very distant phylogenetic bacterial taxa within hosts feeding on similar diets. Despite this similarity, different nitrogen economy strategies have emerged in each case. Both bacterial endosymbionts code for urease but display different metabolic functions: Blochmannia strains produce ammonia from dietary urea and then use it as a source of nitrogen, whereas Blattabacterium strain Bge codes for the complete urea cycle that, in combination with urease, produces ammonia as an end product. Not only does the cockroach endosymbiont play an essential role in nutrient supply to the host, but also in the catabolic use of amino acids and nitrogen excretion, as strongly suggested by the stoichiometric analysis of the inferred metabolic network. Here, we explain the metabolic reasons underlying the enigmatic return of cockroaches to the ancestral ammonotelic state.

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Section: Resultscontrasting

confidence: 78%

“…For instance, uric acid accumulation has been observed in aposymbiotic cockroaches [28],[29]. Metabolic use of nitrogen derived from fat body urates has been observed in B. germanica under certain conditions (e.g., in females on low-protein diet [30] and consumption of empty spermatophores by starved females [31]).…”

Section: Resultsmentioning

confidence: 99%

Evolutionary Convergence and Nitrogen Metabolism in Blattabacterium strain Bge, Primary Endosymbiont of the Cockroach Blattella germanica

et al. 2009

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“…has been hypothesized (6). In the genome sequence of the Blattabacterium symbiont, however, there is no candidate gene for uricolytic enzymes (47), suggesting that the symbiont does not play a role, at least in the initial step of UA utilization.…”

Section: Resultsmentioning

confidence: 99%

“…Not merely regarded as nitrogenous waste, UA is apparently utilized as a nitrogen source or metabolic reserve in some insects, particularly those existing on a nitrogen-poor diet ( e.g. 6, 10, 18, 44). Nitrogen acquisition is a primary concern of insects feeding on diets mostly composed of plant materials.…”

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confidence: 99%

Isolation and Characterization of Anaerobic Bacteria for Symbiotic Recycling of Uric Acid Nitrogen in the Gut of Various Termites

et al. 2012

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Recycling of the nitrogenous waste uric acid (UA) of wood-feeding termites by their gut bacteria is one of the significant aspects of symbiosis for the conservation of nitrogen sources. Diverse anaerobic UA-degrading bacteria comprising 16 species were isolated from the gut of eight termite species, and were assigned to Clostridia, Enterobacteriaceae, and low G+C Gram-positive cocci. UA-degrading Clostridia had never been isolated from termite guts. UA-degrading ability was sporadically distributed among phylogenetically various culturable anaerobic bacteria from termite guts. A strain of Clostridium sp., which was commonly isolated from three termite species and represented a probable new species in cluster XIVa of clostridia, utilized UA as a nitrogen source but not as a sole carbon and energy source. This feature is in clear contrast to that of well-studied purinolytic clostridia or previously isolated UA degraders from termite guts, which also utilize UA as a sole carbon and energy source. Ammonia is the major nitrogenous product of UA degradation. Various purines stimulated the growth of this strain when added to an otherwise growth-limiting, nitrogen poor medium. The bacterial species involved the recycling of UA nitrogen in the gut microbial community of termites are more diverse in terms of both taxonomy and nutritional physiology than previously recognized.

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“…Similarly, Reticulitermes flavipes hindgut bacteria ferment uric acid transported from the fat bodies, via the Malpighian tubules to the hindgut, into ammonia, CO 2 , and acetate (6)(7)(8). Cockroaches, close relatives of termites, harbor intracellular, maternally transmitted bacteria, called Blattabacterium sp., within their fat bodies, near the uric acid deposits (9), and they have been hypothesized to participate in nitrogen recycling from stored uric acid (10,11). Periplaneta americana fat bodies are comprised of two distinct cell types: adipocytes, containing fat globules and uric acid crystals, and mycetocytes, which are filled densely with Blattabacterium (9,(11)(12)(13).…”

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confidence: 99%

Nitrogen recycling and nutritional provisioning byBlattabacterium, the cockroach endosymbiont

Sabree

Kambhampati

Moran

2009

Proc. Natl. Acad. Sci. U.S.A.

261

252

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Nitrogen acquisition and assimilation is a primary concern of insects feeding on diets largely composed of plant material. Reclaiming nitrogen from waste products provides a rich reserve for this limited resource, provided that recycling mechanisms are in place. Cockroaches, unlike most terrestrial insects, excrete waste nitrogen within their fat bodies as uric acids, postulated to be a supplement when dietary nitrogen is limited. The fat bodies of most cockroaches are inhabited by Blattabacterium, which are vertically transmitted, Gram-negative bacteria that have been hypothesized to participate in uric acid degradation, nitrogen assimilation, and nutrient provisioning. We have sequenced completely the Blattabacterium genome from Periplaneta americana. Genomic analysis confirms that Blattabacterium is a member of the Flavobacteriales (Bacteroidetes), with its closest known relative being the endosymbiont Sulcia muelleri, which is found in many sap-feeding insects. Metabolic reconstruction indicates that it lacks recognizable uricolytic enzymes, but it can recycle nitrogen from urea and ammonia, which are uric acid degradation products, into glutamate, using urease and glutamate dehydrogenase. Subsequently, Blattabacterium can produce all of the essential amino acids, various vitamins, and other required compounds from a limited palette of metabolic substrates. The ancient association with Blattabacterium has allowed cockroaches to subsist successfully on nitrogen-poor diets and to exploit nitrogenous wastes, capabilities that are critical to the ecological range and global distribution of cockroach species.Flavobacteria ͉ insect endosymbiont ͉ nitrogen conservation ͉ uricolysis

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Uric acid metabolism by symbiotic bacteria from the fat body of Periplaneta americana

Cited by 39 publications

References 20 publications

Evolutionary Convergence and Nitrogen Metabolism in Blattabacterium strain Bge, Primary Endosymbiont of the Cockroach Blattella germanica

Evolutionary Convergence and Nitrogen Metabolism in Blattabacterium strain Bge, Primary Endosymbiont of the Cockroach Blattella germanica

Isolation and Characterization of Anaerobic Bacteria for Symbiotic Recycling of Uric Acid Nitrogen in the Gut of Various Termites

Nitrogen recycling and nutritional provisioning byBlattabacterium, the cockroach endosymbiont

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