Classification and distribution of large intestinal bacteria in nonhibernating and hibernating leopard frogs (Rana pipiens)

Banas, Jeffrey A.; Loesche, Walter J.; Nace, George W.

doi:10.1128/aem.54.9.2305-2310.1988

Cited by 25 publications

(22 citation statements)

References 14 publications

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“…Populations of gut bacteria commonly are reduced in dormancy and, accordingly, in R. pipiens and R. catesbeiana they fall by 80-90% during underwater hibernation [47][48][49][50]. By contrast, the reduction in our R. sylvatica, a terrestrial hibernator, was only approximately 33%.…”

Section: Discussionmentioning

confidence: 99%

Urea hydrolysis by gut bacteria in a hibernating frog: evidence for urea-nitrogen recycling in Amphibia

et al. 2018

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Gut bacteria that produce urease, the enzyme hydrolysing urea, contribute to nitrogen balance in diverse vertebrates, although the presence of this system of urea-nitrogen recycling in Amphibia is as yet unknown. Our studies of the wood frog (), a terrestrial species that accrues urea in winter, documented robust urease activity by enteric symbionts and hence potential to recoup nitrogen from the urea it produces. Ureolytic capacity in hibernating (non-feeding) frogs, whose guts hosted an approximately 33% smaller bacterial population, exceeded that of active (feeding) frogs, possibly due to an inductive effect of high urea on urease expression and/or remodelling of the microbial community. Furthermore, experimentally augmenting the host's plasma urea increased bacterial urease activity. Bacterial inventories constructed using 16S rRNA sequencing revealed that the assemblages hosted by hibernating and active frogs were equally diverse but markedly differed in community membership and structure. Hibernating frogs hosted a greater relative abundance and richer diversity of genera that possess urease-encoding genes and/or have member taxa that reportedly hydrolyse urea. Bacterial hydrolysis of host-synthesized urea probably permits conservation and repurposing of valuable nitrogen not only in hibernating but, given urea's universal role in amphibian osmoregulation, also in virtually all Amphibia.

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Section: Discussionmentioning

confidence: 99%

Urea hydrolysis by gut bacteria in a hibernating frog: evidence for urea-nitrogen recycling in Amphibia

et al. 2018

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“…For example, the microbiota of four-toed salamanders, Hemidactylium scutatum, include bacteria that inhibit the growth of oophagus fungus and B. dendrobatidis (Harris et al 2006). However, microbiota may vary with environmental conditions, as shown in the large intestine of hibernating and nonhibernating Rana pipiens (Carr et al 1976, Gossling et al 1982, Banas et al 1988). The effectiveness of these innate skin defenses also varies with species.…”

Section: Host Immune Suppression In the Coldmentioning

confidence: 99%

Life-History Trade-Offs Influence Disease in Changing Climates: Strategies of an Amphibian Pathogen

Woodhams

Alford

Briggs

et al. 2008

Ecology

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Life-history trade-offs allow many animals to maintain reproductive fitness across a range of climatic conditions. When used by parasites and pathogens, these strategies may influence patterns of disease in changing climates. The chytrid fungus, Batrachochytrium dendrobatidis, is linked to global declines of amphibian populations. Short-term growth in culture is maximal at 17 degrees-25 degrees C. This has been used in an argument that global warming, which increases the time that amphibians spend at these temperatures in cloud-covered montane environments, has led to extinctions. Here we show that the amphibian chytrid responds to decreasing temperatures with trade-offs that increase fecundity as maturation rate slows and increase infectivity as growth decreases. At 17 degrees-25 degrees C, infectious zoospores encyst (settle and develop a cell wall) and develop into the zoospore-producing stage (zoosporangium) faster, while at 7 degrees-10 degrees C, greater numbers of zoospores are produced per zoosporangium; these remain infectious for a longer period of time. We modeled the population growth of B. dendrobatidis through time at various temperatures using delayed differential equations and observational data for four parameters: developmental rate of thalli, fecundity, rate of zoospore encystment, and rate of zoospore survival. From the models, it is clear that life-history trade-offs allow B. dendrobatidis to maintain a relatively high long-term growth rate at low temperatures, so that it maintains high fitness across a range of temperatures. When a seven-day cold shock is simulated, the outcome is intermediate between the two constant temperature regimes, and in culture, a sudden drop in temperature induces zoospore release. These trade-offs can be ecologically important for a variety of organisms with complex life histories, including pathogenic microorganisms. The effect of temperature on amphibian mortality will depend on the interaction between fungal growth and host immune function and will be modified by host ecology, behavior, and life history. These results demonstrate that B. dendrobatidis populations can grow at high rates across a broad range of environmental temperatures and help to explain why it is so successful in cold montane environments.

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“…Frogs normally feed on crickets, and thus the intestinal flora would be accustomed to a protein-rich diet, which would account for the ability of the suspensions of the intestinal flora to utilize substrates, such as amino acids and glycoproteins, as opposed to simple carbohydrates, such as galactose, fucose, or glucose. These results were not surprising given that the majority of individual bacterial isolates from nonhibernators did not utilize glucose (4) and those that did were mainly enterobacteria. Few of the anaerobic isolates, whether Bacteroides or Clostridium spp., were saccharolytic, a finding which differs markedly from results obtained with mammals, in which the large proportion of Bacteroides species in the colon are saccharolytic (27,31).…”

Section: Discussionmentioning

confidence: 90%

“…Of four frogs tested with glucose, none was positive. and hibernators in that anaerobes dominated in the nonhibernators and facultative bacteria accounted for about half the flora in the hibernators (4).…”

Section: Resultsmentioning

confidence: 99%

“…The large intestinal flora in hibernating frogs is significantly different from the flora in nonhibernators (4) in that a lower concentration of bacteria is present and there is a greater proportion of facultative psychrophiles and facultative anaerobic and aerobic bacteria, especially pseudomonads. The selective pressure of low temperature is probably responsible for the increased proportion of psychrophiles.…”

mentioning

confidence: 88%

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Possible mechanisms responsible for the reduced intestinal flora in hibernating leopard frogs (Rana pipiens)

Banas

Loesche

Nace

1988

Appl Environ Microbiol

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Mechanisms and factors that normally control the large intestinal flora were investigated to determine whether changes in these parameters could account for the decreased bacterial concentration and facultative nature of the flora found in hibernating frogs. It appeared that low temperatures and limited nutrients were the main factors responsible for the decrease in the bacterial concentration and may also have been responsible for the increase in the proportions of facultative organisms, since no change in the redox potential was seen. The hibernating frogs were extremely sluggish in the removal of India ink particles from the circulatory system by the Kupifer cells of the liver compared with nonhibernating frogs. They were unable to mount an antibody response to bovine serum albumin, but their serum did exhibit killing of Pseudomonas paucimobilis, suggesting opsonization by preformed antibody and complement. The role of these host factors in protecting the hibernating frog against this indigenous flora is discussed.

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Classification and distribution of large intestinal bacteria in nonhibernating and hibernating leopard frogs (Rana pipiens)

Cited by 25 publications

References 14 publications

Urea hydrolysis by gut bacteria in a hibernating frog: evidence for urea-nitrogen recycling in Amphibia

Urea hydrolysis by gut bacteria in a hibernating frog: evidence for urea-nitrogen recycling in Amphibia

Life-History Trade-Offs Influence Disease in Changing Climates: Strategies of an Amphibian Pathogen

Possible mechanisms responsible for the reduced intestinal flora in hibernating leopard frogs (Rana pipiens)

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