Nitrogen fixing bacteria in the gut of Panaque nigrolineatus

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Nitrogen fixing bacteria in the gut of Panaque nigrolineatus

Post by bekateen »

McDonald, R., Zhang, F., Watts, J. E. M., & Schreier, H. J. 2015. Nitrogenase diversity and activity in the gastrointestinal tract of the wood-eating catfish Panaque nigrolineatus. The ISME Journal, (24 April 2015) | http://dx.doi.org/10.1038/ismej.2015.65

ABSTRACT
The Amazonian catfish, , consume large amounts of wood in their diets. The nitrogen-fixing community within the gastrointestinal (GI) tract of these catfish was found to include nifH phylotypes that are closely related to Clostridium sp., Alpha and Gammaproteobacteria, and sequences associated with GI tracts of lower termites. Fish fed a diet of sterilized palm wood were found to contain nifH messenger RNA within their GI tracts, displaying high sequence similarity to the nitrogen-fixing Bradyrhizobium group. Nitrogenase activity, measured by acetylene reduction assays, could be detected in freshly dissected GI tract material and also from anaerobic enrichment cultures propagated in nitrogen-free enrichment media; nifH sequences retrieved from these cultures were dominated by Klebsiella- and Clostridium-like sequences. Microscopic examination using catalyzed reporter deposition-enhanced immunofluorescence revealed high densities of nitrogenase-containing cells colonizing the woody digesta within the GI tract, as well as cells residing within the intestinal mucous layer. Our findings suggest that the P. nigrolineatus GI tract provides a suitable environment for nitrogen fixation that may facilitate production of reduced nitrogen by the resident microbial population under nitrogen limiting conditions. Whether this community is providing reduced nitrogen to the host in an active or passive manner and whether it is present in a permanent or transient relationship remains to be determined. The intake of a cellulose rich diet and the presence of a suitable environment for nitrogen fixation suggest that the GI tract microbial community may allow a unique trophic niche for P. nigrolineatus among fish.

Cheers, Eric

P.S. Articles like this continually remind me of the importance of natural bacteria living in the digestive tracts of animals, and it's also a reminder that we shouldn't overuse antibiotics.

EDIT: This paper follows from another paper from the same lab, cited previously in this forum ("Gut microbes in Panaque," viewtopic.php?f=14&t=37335). And, without intending to express a personal opinion/comment on the issue, the inaccessibility of the new paper is in stark contrast to the open access nature of the earlier article. -Eric
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Re: Nitrogen fixing bacteria in the gut of Panaque nigrolineatus

Post by yannick62 »

Very interesting article....
Thank you
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Re: Nitrogen fixing bacteria in the gut of Panaque nigrolineatus

Post by Bas Pels »

citate
The intake of a cellulose rich diet and the presence of a suitable environment for nitrogen fixation suggest that the GI tract microbial community may allow a unique trophic niche for P. nigrolineatus among fish.
end of citate

Now I wonder, what advantage could this fish possibly have by hosting these bacteria? Nitrogen fixating results in ammonia or nitrate - compounds a fish rather gets rid of. Fish are, just as all other animals, not able to turn nitrate or ammonia into amino acids - only plants, and perhaps bacteria are able to do this

So any advantage must rely in the existence of bacteria which turn these nitrogen into amino acids - better out, proteins. But that would imply that these bacteria are digested, and the bacteria living in the gut are safe, as digesting of cells takes place in the stomach

Can anybody explain what I am missing? I do agree a diet of wood might be low in protein - but Panaque does not eat wood, but the bacteria rotting the wood - that is, they actually may have a rather protein rich diet
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Re: Nitrogen fixing bacteria in the gut of Panaque nigrolineatus

Post by matthewfaulkner »

Has anyone got a copy of this to share? I can't seem to access it as usual.
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Re: Nitrogen fixing bacteria in the gut of Panaque nigrolineatus

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Re: Nitrogen fixing bacteria in the gut of Panaque nigrolineatus

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Bas Pels wrote:Now I wonder, what advantage could this fish possibly have by hosting these bacteria? Nitrogen fixating results in ammonia or nitrate - compounds a fish rather gets rid of. Fish are, just as all other animals, not able to turn nitrate or ammonia into amino acids - only plants, and perhaps bacteria are able to do this

So any advantage must rely in the existence of bacteria which turn these nitrogen into amino acids - better out, proteins. But that would imply that these bacteria are digested, and the bacteria living in the gut are safe, as digesting of cells takes place in the stomach

Can anybody explain what I am missing? I do agree a diet of wood might be low in protein - but Panaque does not eat wood, but the bacteria rotting the wood - that is, they actually may have a rather protein rich diet
If I understand your concern, the issue is that these microbes are housed in areas of the gut after the stomach, and therefore they should not be subject to cellular digestion, and as a result the panaque would get little nutritional benefit (in terms of useful nitrogenous compounds like amino acids) from housing these microbes and providing them an environment where the microbes can breed. That makes sense, since the primary examples of vertebrates relying on microbial digestion are the ungulates (like cows) with microbes in the stomach, and coprophages (like rabbits) which have a post-intestinal bacterial cecum, requiring these animals to eat their own feces to recover the nutrients.

I have three observations on this, none of which conclusively addresses the issue, but they may help shine some light on the issue: First, if you look at insects like termites, they do house many of their gut microbes in the hindgut, not the foregut. Second, in this paper the authors make no mention of the auxiliary lobe in the panaque's digestive tract, but their earlier paper does. Perhaps that is involved in the process of nutrient recovery from these microbes (I have no idea, just speculating). And finally, do adult panaques perform any coprophagy in nature? I know we all try to keep our tanks clean by vacuuming the substrate, but I've see my baby albino BNs voraciously eat the feces of their parents, especially after the parents have been feeding on raw sweet potato. I've wondered about how important this practice is to the nutritional health and growth rate of the juveniles; if it is important, then leaving some poop on the tank bottom for the growing babies may be a good thing, as long as water quality is maintained... that's just a thought, although I may be way off base here. (note: the image doesn't show the babies feeding, but it shows the orange and brown fecal droppings of mom, dad, and all the fry before I vacuumed them up; the fry are often in the middle of this eating)Image
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Re: Nitrogen fixing bacteria in the gut of Panaque nigrolineatus

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McDonald, R., Zhang, F., Watts, J. E. M., & Schreier, H. J. wrote:The Amazonian catfish,
I wonder which species they really investigated.

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Re: Nitrogen fixing bacteria in the gut of Panaque nigrolineatus

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Jools wrote:I wonder which species they really investigated.
Quoting the authors' Materials & Methods,
Wild-caught P. nigrolineatus (L-190) were imported from South America by the fish wholesaler Aquascapeonline (Belleville, NJ, USA).
If you go back and examine their earlier paper on these fish, they wrote this:
Panaque nigrolineatus (L-190) were imported from the Peruvian Amazon jungle basin from the fish wholesaler Aquascapesonline (Belleville, NJ)
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Re: Nitrogen fixing bacteria in the gut of Panaque nigrolineatus

Post by Bas Pels »

@ bekateen, parents housing bacteria in their gut in order to have their offspring grow better would be something of another example of how nature can cope with problems. I think it would suit the finding that very young Panaque are muchmore sensitive then their elders

@ Jools, Good point. Long ago, in 1991/2 as a student, I was working with Oreochromis mossambica. I did not exactly have to tell them they were not Tilapia anymore - but the general feeling was that the new name was rather inconvenient. My explaining that Oreochromis are mouth breeders and Tilapia substrate breeders, that the species are not that related was clearly not something they were interested in. That day I learned that fysiologists are not that interested in taxonomy - a branch which they hardly consider a science. But I have to admit, these fysiologists do work which is not reproducible - for lack of information regarding the kind of animal they use. And not reproducible work is worse than nothing.

Betateen, The Peruvian jungle is rather large, is it not? I wrote the above and then saw your posting, but I do feel the work could be more valuable if they had used fish they knew more about.
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Re: Nitrogen fixing bacteria in the gut of Panaque nigrolineatus

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Hi Bas Pels,
Bas Pels wrote:@ bekateen, parents housing bacteria in their gut in order to have their offspring grow better would be something of another example of how nature can cope with problems. I think it would suit the finding that very young Panaque are muchmore sensitive then their elders
Yes, I think that would be an interesting experiment in itself - how does the microbial population of juveniles (esp. really young ones) compare to that of the adults? And how are the juveniles affected nutritionally and in growth rate (positively or negatively) if they are given or deprived access to parental feces as a food source?
Bas Pels wrote:That day I learned that fysiologists are not that interested in taxonomy - a branch which they hardly consider a science. But I have to admit, these fysiologists do work which is not reproducible - for lack of information regarding the kind of animal they use. And not reproducible work is worse than nothing.
While I appreciate your point, and there is certainly plenty of evidence for your idea if we look back at the history of physiological publications, I must also take issue with your perspective, speaking as a comparative physiologist myself.

First, I disagree with the general notion that physiologists "hardly consider [taxonomy] a science." IME, the physiologists I've trained under and worked with cared quite a bit about the taxonomy of the animals they used. But they often don't have the skills or tools to exercise a thorough investigation of the exact species (or subspecies, etc.) identity of the animals they use; here I agree with you that the shortcoming should not be ignored, but it often doesn't reflect an overt disinterest in taxonomy or its relevance.

Second, physiologists often obtain animals without a complete explanation of the animal's origin/source. While that's not good, it does not automatically negate the value of the research. For example, as part of my dissertation, I used a frog named Rana pipiens. This species is a taxonomic nightmare; it is not one species but a species complex; the boundaries between the various species and subspecies all called R. pipiens was poorly defined at the time of my dissertation work. But none-the-less, I was able to document some very interesting and novel details about the skin of this frog and I got most of that work published. Unfortunately, I couldn't say anything about the source of my actual frogs, other than the name of the supplier who sold them to me (just as these authors did)... and who knows where all of their specimens were from. My point is this: I had some frogs; I used them in some competently-designed experiments, and I obtained some significant results that brought a fresh perspective to an old subject, even though I couldn't say whether my frogs were R. pipiens or one of 30 other species in the pipiens complex. I called them R. pipiens in my papers; I might be wrong about the species ID, but that doesn't make me wrong about what I learned regarding the skin of these frogs. And since my paper was a comparative paper using other frog species too, the results from this one group of "R. pipiens" were placed in the context of a bigger picture. So in defense of these papers, the authors may not have a clue which particular panaque they used. But if they, or anyone else continues to pursue this subject, the bacterial data provided in these papers will be invaluable. And here's where I think I really disagree with you: I disagree with your statement that this work falls to the low quality of "And not reproducible work is worse than nothing." You may not be able to find their exact fish and reproduce this, but if the molecular biology and bacteriology is sound, you can go out and get your own panaques, or any other loricariids, with all the proper documentation you can get, and what you find can be compared back to this data. (that said, I am not defending or excusing the authors for not having better information - see below).
Bas Pels wrote:Betateen, The Peruvian jungle is rather large, is it not? I wrote the above and then saw your posting, but I do feel the work could be more valuable if they had used fish they knew more about.
I agree fully. I was not posting these quotes to defend the authors, but simply to provide Jools with as much info as the authors gave us on the issue of origin.

Cheers, Eric
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Re: Nitrogen fixing bacteria in the gut of Panaque nigrolineatus

Post by matthewfaulkner »

Jools wrote:I wonder which species they really investigated.
This is what I wondered in the 2013 paper as well. This is the quote from the materials section - "P. nigrolineatus were imported from Rio Xingu, Peru, through commercial wholesale distributors (AquaScape Online, Belleville, NJ, USA)."

From that statement, the identity of the specimens could be one of three different species - , or . Out of the three, I think P. nigrolineatus is the most likely, primarily due to it's availability and comparatively lower price (P. titan/L418 is rarely seen in the trade, and P. cf. armbrusteri was probably still prohibited at that time).

I think the results would be more even more interesting if the fish were actually P. cf. armbrusteri.
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Re: Nitrogen fixing bacteria in the gut of Panaque nigrolineatus

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matthewfaulkner wrote:From that statement, the identity of the specimens could be one of three different species - , or . Out of the three, I think P. nigrolineatus is the most likely, primarily due to it's availability and comparatively lower price (P. titan/L418 is rarely seen in the trade, and P. cf. armbrusteri was probably still prohibited at that time).

I think the results would be more even more interesting if the fish were actually P. cf. armbrusteri.
This intrigues me, as I have no experience with panaques. Matthew, your statement makes me wonder two things:
  1. What is it about P. cf. armbrusteri that would make these results more interesting to you? Is it merely that so little is known about this particular fish? Or is there something special about the biology/ecology/diet of this particular fish that would be uniquely enlightened by the knowledge developed by these authors?
  2. More generally speaking, in your opinion (or anyone else could answer this), how would your interpretation of the results be influenced by knowing specifically which panaque was used by these authors? In other words, what is different about the biology/ecology/diet of each of these species that could be included in the analysis done by these authors, and thus add value to the paper? Said another way, now that you know what these authors have discovered, what questions would you like to pursue next if you were given the chance to participate in this research? Where would you go with this project?
Please don't misinterpret these questions; I'm not asking in a critical sense, but rather to better understand the diversity of this group of fishes, and to explore the subject with my own curiosity. :-)

Cheers, Eric

P.S., As a scientist, I am always fascinated to dive into biology and explore the fine details of how various organisms have adapted to their unique habitats. And these papers, even given any potential weakness due to an ambiguity about fish ID, are intriguing for exactly this reason. None-the-less, off the top of my head, I can't think of a single vertebrate organism which thrives on a diet consisting primarily of tough, fibrous primary growth plant matter and old-growth plant matter (i.e., wood) WITHOUT also being dependent on a rich flora of gastrointestinal microorganisms capable of digesting these foods on behalf of the animal host and then providing essential nutrients to the host. In that sense, without being disrespectful to the authors, I'm experiencing a slight "Of course, what else?" moment - Shouldn't this result be expected?
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Re: Nitrogen fixing bacteria in the gut of Panaque nigrolineatus

Post by Acanthicus »

Morning everybody,

there is a huge difference in the diet concerning P. cf. armbrusteri and the P. nigrolineatus complex. First mentioned don't feed as much on wood as we believed for years. In fact there is no wood at all in the natural habitat. When I collected P. cf. armbrusteri in Xingu the first time I expected them to live on or at least nearby fallen trees or something similar. But it turned out they live in a pure stone biotope, without any wood! Nothing surprising if you look at the teeth, they are very different from the ones P. nigrolineatus use to have, but still Panaque are generally considered woodeaters, but not all are. Having in mind two different diets it seems logical that the bacterial fauna is different as well, and thats why it would be great to know the examined species for sure.

cheers, Daniel
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Re: Nitrogen fixing bacteria in the gut of Panaque nigrolineatus

Post by bekateen »

Yes, this is the kind of info that shines light on this paper. Thank you, Daniel. Now, considering this information, I'd still expect a plant/algae eating fish to have some (not all) of the same dietary needs for digestive microbes as I would find in a wood-eating fish. I mean, cows and rabbits obviously aren't primarily wood eaters, but they can become malnourished if their gut flora are killed off by antibiotics. So should N-fixing bacteria be as important to an algae/plant eater as they might be to a wood eater? (of course, this assumes the authors' premise that there is a nitrogen benefit to the fish host from the N-fixing bacteria found in their study).

Cheers, Eric

EDIT: This also makes me wonder whether or not the authors of these papers have saved any tissue from the fish they used which might be used to develop a genetic fingerprint, thus providing (after the fact) a better identification.
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Re: Nitrogen fixing bacteria in the gut of Panaque nigrolineatus

Post by matthewfaulkner »

bekateen wrote:
  1. What is it about P. cf. armbrusteri that would make these results more interesting to you?
  2. More generally speaking, in your opinion (or anyone else could answer this), how would your interpretation of the results be influenced by knowing specifically which panaque was used by these authors?
I just want to preface this with that I still think the fish used were likely P. nigrolineatus (or at least a similar species/variety), rather than P. cf. armbrusteri 'Xingu'.
  1. Just like Daniel/Acanthicus said, because their habitat seems to be devoid of wood to feed on, and that they possess a unique ontogenetic increase in the number of teeth and teeth row angle (Lujan et al. 2010); meaning that they are less well adapted to gouging wood and more similar to the majority of auwfuchs grazers.
  2. I think the results would be more significant because P. cf. armbrusteri seems to have diverged from the main block of wood eating Panaque, yet they retain these nitrogen fixing microbial communities beneficial to 'wood eating', despite their physiology and ecology being different.

Aside from this specific topic of identity and more on the overall topic, I find that I struggle with cognitive dissonance over Donovan German's work saying that their GI tract is not specialised for 'wood eating' and that McDonald, Watts etc work says that their GI tract is.

Lujan, Hidalgo & Stewart. (2010). Revision of Panaque (Panaque), with Descriptions of Three New Species from the Amazon Basin (Siluriformes, Loricariidae). doi:10.1643/CI-09-185
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Re: Nitrogen fixing bacteria in the gut of Panaque nigrolineatus

Post by bekateen »

Thank you Matthew, that is also very interesting.

As to your cognitive dissonance, yes, that will be difficult to resolve. If these panaques aren't fermenting xylophages, why would they have all the wood-digesting and nitrogen-fixing bacteria?

I'm still wondering about the prospect of coprophagy, although I imagine that this would be less likely in a flowing stream, where feces are continuously washed away, than it would be in an aquarium; so this is probably not very likely in nature.

And then there's the function of this "accessory lobe" (AL) organ in the panaque intestinal tract - is it functioning at all like a fermentation chamber? I can't find much about the AL; so far, besides these papers, the only reference I'm finding comes from a biology thesis: Dehn, A. 2010. Physiological, histological, and morphological evidence of microbial symbiosis in a xylophagous catfish Panaque nigrolineatus. Biology Thesis Towson: Towson University.
ABSTRACT wrote:Fish of the genus Panaque (Loricariidae) are known to be xylophagic, or wood consuming, although evidence for nutrient assimilation from wood is sparse. To determine if gut bacteria are involved in a mutualistic endosymbiosis in which P. nigrolineatus gain energy from wood, growth trials on restricted diets of palm wood in combination with analysis of indicators of bacterial fermentation were conducted. While most individuals did not exhibit positive growth, the mean loss in body mass over 28 d was minimal (2.14 - 4.23%). Analysis of short chain fatty acids (SCFAs) in the intestine revealed a profile that was (1) dominated by acetate, (2) increased distally along the GI tract, and (3) contained enough acetate to potentially meet the basal metabolic demands of P. nigrolineatus.

Upon histological examination of the intestine, large conglomerates of bacteria were seen along the dense epithelial brush border and surrounding the digesta in the lumen. Examination of the gross morphology revealed a relative intestine length = 11, a highly coiled intestine, and a loop reversal occurring at 52% of the intestine length distal to the stomach, resulting in countercurrent flow of digesta .

The physiological, histological, and morphological observations seen in P. nigrolineatus are consistent with those of other herbivorous teleosts that rely on bacterial endosymbionts for nutrient acquisition.
I've requested a copy of this thesis by Interlibrary Loan from my university. Hopefully the request is granted and the thesis doesn't take too long to arrive. :-SS :-b

To add to your confusion, there is this abstract from a poster presentation: PRODUCTION OF CELLULOLYTIC ENZYMES BY A MICROBIAL COMMUNITY ISOLATED FROM A WOOD-EATING CATFISH GASTRO-INTENSTINAL TRACT by Rebecca E. Kulp & Damian Smoot. Look at the last lines of that abstract:
Preliminary results from the enzyme assays show that the microbial communities isolated from fish on both diets produced enzymes directed against recalcitrant carbon-carbon bonds like those found in wood. Bacterial isolates also showed the highest enzyme activity against the ß-glucosidase bond. Yet, fish on the wood-only diet lost 8.7% of their body weight, whereas, fish on the algae diet gained 38% of their body weight.

Both of the above sources found weight loss in panaques fed wood-only diets.

After reading all this, it makes me wonder all the more which panaques they are studying. It would make sense that algae/plant-eating panaques might lose weight if forced onto a wood-only diet, but I wouldn't expect a wood-eating panaque to lose weight, as long as the experimental diet is consistent with any natural wood diet they were eating prior to capture.

On the other hand, weight loss in either of these studies might be relatively meaningless, IF the authors were inadvertently feeding the panaques a nutrient-rich diet in between the time of capture and the start of experimental analysis, because such an unnatural diet might lead to abnormal weight gain... And then, when the fish are transitioned onto an experimental wood-only diet, their bodies would be forced to re-adapt to a calorie- and nutrient restricted diet, and they might loose any recent weight gain. I guess I would want to reexamine the individual body masses at the time of capture, the food regimen between capture and experimentation, and the body mass at the start and end of experimentation, for starters.

I'm sure I'm overlooking many details, but these issues come to the forefront of my mind.

Cheers, Eric

P.S. By the way, the 2009 paper by Donovan German and Rosalie Bittong does a much better job of documenting the source of the panaques used in the research than do the other papers discussed in this thread:
German & Bittong wrote:Ten adult individuals each of Panaque cf. nigrolineatus “Marañon” and P. nocturnus, and five adult individuals of Hypostomus pyrineusi were captured by seine and a backpack electroshocker from the upper Río Marañon in northern Peru (4°58.957'S, 77°85.283'W) in August 2006.
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Re: Nitrogen fixing bacteria in the gut of Panaque nigrolineatus

Post by bekateen »

bekateen wrote:Quoting the authors' Materials & Methods,
Wild-caught P. nigrolineatus (L-190) were imported from South America by the fish wholesaler Aquascapeonline (Belleville, NJ, USA).
If you go back and examine their earlier paper on these fish, they wrote this:
Panaque nigrolineatus (L-190) were imported from the Peruvian Amazon jungle basin from the fish wholesaler Aquascapesonline (Belleville, NJ)
Did anybody happen to look at the importer's website (http://www.aquascapeonline.com/prodList ... ategory=86)? It appears that, at least at this moment, the importer has several different panaques listed (but not currently in stock). So maybe, if the importer knows the difference, and if the authors bought "nigrolineatus" from the importer, then maybe there's a chance that these authors actually got real nigrolineatus.

We (and they) should be so lucky.

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Re: Nitrogen fixing bacteria in the gut of Panaque nigrolineatus

Post by TwoTankAmin »

As a non-scientist, I have been reading this thread and not commenting. But I am a bit confused about two things and if one of the better educated folks in this thread might be able to clear things up for me. The fist concerns the identity of the fish involved. Last time I looked at a map, no part of the Xingu is in Peru. When I peruse the cat-e-logue here all of the rivers listed for Panaque nigrolineatus are not anywhere near Peru and the L number is 190. When I check the Aquascape Online site, they show in stock Panaque bathyphilus as L90 (http://www.aquascapeonline.com/prodList ... tegory=636), Panaque sp. (L191) and Panaque cf. armbrusteri`xingu` L27. If the cat-e-log is correct only Panaque bathyphilus L90 is found in Peru. So I am completely confused as to which fish they were examining. From what I read in this thread it and what Aquascape online states, it appears to me as if the fish being examined is Panaque bathyphilus and not nigrolineatus. Can anybody unconfuse me or correct what I thought I saw to be the case?

The other thing that I wondered about is how the bacteria in question got into the fish. If I understand correctly this would be only one of two ways. Either they are born with them or else they must acquire them via their diet. If the method of introduction is the latter, this would suggest they are consumed when the fish rasps the wood, as it is also eating the biofilm which would contain these bacteria. If the bacteria are required, babies might consume some of the parents feces to acquire them much the same way baby elephants eat their parents dung to introduced needed gut bacteria. But if these bacteria are not essential but are acquired as a by product of consuming wood etc., how long might these bacteria be present in the digestive tract even if the fish were prevented from consuming them by controlling their diet. What I am wondering is if these bacteria are essential for the fish to have or if they are there and functioning more or a less due to their having been consumed and their surviving but are not an essentially required aid to some other process. Is it possible that they contribute little to the fish but are there as a sort of "side effect?" From what I read in the thread and from looking at some of the research mentioned, I saw no conclusions about what function these bacteria played in contributing to the fish's well being or dietary needs. Did I miss something here?

Sorry for intruding on a scientific thread without having the education to understand it all. I am just curious as well as ignorant here.
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Re: Nitrogen fixing bacteria in the gut of Panaque nigrolineatus

Post by bekateen »

Hi TTA,
TwoTankAmin wrote:As a non-scientist, I have been reading this thread and not commenting. But I am a bit confused about two things and if one of the better educated folks in this thread might be able to clear things up for me.

Sorry for intruding on a scientific thread without having the education to understand it all. I am just curious as well as ignorant here.
Please, don't feel inhibited about jumping in. In fact, I think you hold your own very well when discussing the extremely tiny details of many subjects. Your past comments to me and others about nitrogen-metabolizing prokaryotes (bacteria and archaeans) led me to believe that your profession and/or education was in the field of microbiology. So it's a bit of a surprise to me to read that you are a "non-scientist." ^:)^ Honestly, there's nothing magical about being a scientist.
TwoTankAmin wrote:The other thing that I wondered about is how the bacteria in question got into the fish. If I understand correctly this would be only one of two ways. Either they are born with them or else they must acquire them via their diet.
Of the two choices you presented (born with microbes or acquire them), the second is undoubtedly the explanation. To my knowledge, a fish egg cannot be laid with microbes "inside" of it, since the egg is a single cell (EDIT: Some microbes could be deposited on the jelly coat outside the egg at the time of laying, since the eggs and feces all exit mom's body through the same opening, the cloaca; but I don't see that as being a major source). So at some point in the growth of the fry, the fry ingests various microbes and these colonize its digestive tract. Humans are no different; there is a veritable menagerie of microbes living in the human gut, the community diversity varies from one segment of our gut to the next, and we are only now beginning to think about how these microbes help us (e.g., read, C.J. Robinson, B.J.M. Bohannan and V.B. Young. 2010. From Structure to Function: the Ecology of Host-Associated Microbial Communities. Microbiol. Mol. Biol. Rev. 74(3):453. DOI: 10.1128/MMBR.00014-10; or read J.Schrezenmeir and M. de Vrese. 2001. Probiotics, prebiotics, and synbiotics—approaching a definition. Am J Clin Nutr, 73(suppl):361S–4S (it's dated, but still good)). One of the take-home lessons I get from these papers is that each animal's digestive tract can be thought of as a big apartment building, and one way or another, every "apartment" in the building will get occupied by microbes. If the gut is filled with microbes that are beneficial or at least harmless, then it becomes more difficult for harmful microbes to colonize and establish themselves in the gut, where they can do us harm. For this reason, all animals' digestive tracts can be defined by the microbes that live inside, which the animal either tolerates or benefits from, if for no other reason than the animal avoids colonization by pathogenic microbes.
TwoTankAmin wrote:If the method of introduction is the latter, this would suggest they are consumed when the fish rasps the wood, as it is also eating the biofilm which would contain these bacteria. If the bacteria are required, babies might consume some of the parents feces to acquire them much the same way baby elephants eat their parents dung to introduced needed gut bacteria.
Yes. The same principle which I described for humans undoubtedly applies to these panaques. IMO, it won't matter if the microbes are "required" or not -- either the microbes will be ingested by eating the the wood, or by (intentionally or coincidentally) ingesting fecal matter from adult panaques (or by both means).
TwoTankAmin wrote:But if these bacteria are not essential but are acquired as a by product of consuming wood etc., how long might these bacteria be present in the digestive tract even if the fish were prevented from consuming them by controlling their diet.
I would describe it this way (again, I am writing in general terms, since as you point out, it is obvious that the research on these panaques is not complete): The microbial community living inside an animal's gut is a dynamic community: the variety of species present and the relative abundance of each species change over time for a variety of reasons, one of which is the diet of the animal. So if we transfer a panaque from a natural wood diet onto an algae diet (or vice versa), then we should expect to see a change in the microbial diversity in that animal's gut, WHETHER OR NOT the microbes are essential to the wellness of the panaque. This will be a natural consequence because by changing the animal's diet, we alter the variety and concentrations of various nutrient chemicals in the diet; these changes will favor certain species of microbes, and negatively affect the growth of other species of microbes (essentially changing some of the tenants in our "apartment building").

That said, you also can't predict that by changing the panaques from one food to another that the beneficial bacteria (those relying on a wood diet) will completely die off. Many microbes have the ability to change their metabolic pathways rapidly in response to alterations in food supply. So if they are used to fermenting wood and the wood disappears from the panaque gut, the microbes might be able to alter which enzymes they are expressing and adapt to whatever new foods they are exposed to. So we can't simply ask, if we remove the wood diet, how long will it take for the beneficial microbes to disappear?
TwoTankAmin wrote:What I am wondering is if these bacteria are essential for the fish to have or if they are there and functioning more or a less due to their having been consumed and their surviving but are not an essentially required aid to some other process. Is it possible that they contribute little to the fish but are there as a sort of "side effect?" From what I read in the thread and from looking at some of the research mentioned, I saw no conclusions about what function these bacteria played in contributing to the fish's well being or dietary needs. Did I miss something here?
No, I don't think you missed anything at all. But unfortunately, it won't be that simple.

In vertebrate physiology, we tend to look for gut microbes located in a part of the gut located PRIOR to the place where acidic and enzymatic digestion occurs, because that's the only way microbes can be broken down for the animal to then absorb the nutrients from the microbe. But we are seeing more and more examples in animals, especially in invertebrates, where gut microbes populate the latter parts of the gut, AFTER the digestive regions, and the animals still gain some benefit.

For example, 20-30 years ago, we didn't think (or at least I wasn't taught) that in humans, colonic microbes contributed much to our primary nutrition (giving us more macronutrients like amino acids, sugars, and fats). It was pretty obvious that our colonic microbes were an invaluable source of certain vitamins. And as mentioned in the "apartment building" analogy, if nothing else, our "beneficial" gut microbes reduce the chance that pathogenic microbes will invade. But now we understand that these colonic microbes actually do provide macronutrients that are available to us through metabolism and absorption (e.g., see Wong JM, de Souza R, Kendall CW, Emam A, & Jenkins DJ. 2006. Colonic health: fermentation and short chain fatty acids. J Clin Gastroenterol. 40(3), 235-43.)

So IMO, even though these microbes are "in the wrong place" (mid- and hindgut, rather than foregut) for typical macronutrient access to these panaques, it's still very likely that these microbes are providing significant benefit to the fish. But as yet, the evidence doesn't show one way or another that these microbes are providing a SPECIFIC benefit to the panaques. This is consistent with my earlier comments about the two papers showing weight loss when fed an all-wood diet. I mean, wood is clearly a more challenging food source than algae for these panaques, as a source of proteins and other easily digestible nutrients. So I am not surprised to see weight loss when comparing panaques on wood diets to panaques on algae diets. But that doesn't mean the microbes are useless. What I would like to see is a comparison of two groups of panaques, both eating wood-only diets, with one group of panaques having their gut microbes killed with strong antibiotics and the other group left alone, with a full set of gut microbes. These types of study were conducted decades ago in vertebrates like cows, rabbits, etc., and they showed that without the microbes, the animals became malnourished. If tested on panaques, I would predict that the panaques lose weight faster if they don't have a healthy population of gut microbes, and I would expect that panaques with gut microbes would be (overall) healthier than panaques without. Of course, that's just my hypothesis in the context of the work presented in these papers.

Cheers, Eric
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Re: Nitrogen fixing bacteria in the gut of Panaque nigrolineatus

Post by Suckermouth »

Really interesting discussion, I'd appreciate a PDF of this paper, please!

EDIT: Received, thanks!
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Re: Nitrogen fixing bacteria in the gut of Panaque nigrolineatus

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PM sent.
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Re: Nitrogen fixing bacteria in the gut of Panaque nigrolineatus

Post by matthewfaulkner »

Both of these seem to be from students of Towson University, working with Jay Nelson. Pretty much all the work I've seen from Nelson/Towson Uni has been using .

I noticed that in the main paper we're discussing (McDonald et al. 2015), Jay Nelson is credited for "assistance with fish maintenance."

Nelson also worked with a member here (H.N) and produced - Dietary histories of herbivorous loricariid catfishes: evidence from d13C values of otoliths. The fish used were 'P. nigrolineatus' collected from the Rio do Peixe, Aruana, Goias, Brazil. So, they were likely (also not helping, is that I've seen anecdotal evidence that there are at least two forms of Panaque from the rio Araguaia, both resembling P. cf. armbrusteri and P. cf. nigrolineatus).
TwoTankAmin wrote: But I am a bit confused about two things and if one of the better educated folks in this thread might be able to clear things up for me. The fist concerns the identity of the fish involved. Last time I looked at a map, no part of the Xingu is in Peru. When I peruse the cat-e-logue here all of the rivers listed for Panaque nigrolineatus are not anywhere near Peru and the L number is 190. When I check the Aquascape Online site, they show in stock Panaque bathyphilus as L90, Panaque sp. (L191) and Panaque cf. armbrusteri`xingu` L27. If the cat-e-log is correct only Panaque bathyphilus L90 is found in Peru. So I am completely confused as to which fish they were examining. From what I read in this thread it and what Aquascape online states, it appears to me as if the fish being examined is Panaque bathyphilus and not nigrolineatus. Can anybody unconfuse me or correct what I thought I saw to be the case?
There is Panaque sp. L418 (now absorbed into ) from the rio Huallaga and Maranon in Peru (which is the 'species' that Donovan German used in his work). But I didn't even consider that it could be , so thanks for suggesting it :). I probably discounted it because they are so different to the 'royal' Panaque group. Surely just a google search would make that obvious. I suppose that is also a possibility given that in their earliest paper (McDonald, 2012) they said the fish were collected from the Peruvian Amazon.

But perhaps the authors only dealt with tissue samples sent to them, never having seen the fish they were from, so just relying on the ID from where they originated. Not having any experience with this sort of work/research, is this a possibility?

Now after having written all this (for a lengthy time period that I'm not willing to admit X_X ), I think that my point was that, given Jay Nelson's involvement, my confidence is somewhat restored and these fish are P. nigrolineatus or P. cf. nigrolineatus.
TwoTankAmin wrote: Sorry for intruding on a scientific thread without having the education to understand it all. I am just curious as well as ignorant here.
This is exactly how I feel, being a twice failed uni student myself, I find it intimidating to be in a conversation with those who are PhD, MSc, etc.
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Re: Nitrogen fixing bacteria in the gut of Panaque nigrolineatus

Post by TwoTankAmin »

Eric thank you for both your kind words and your explanations.

While I am not a scientist, I have some background from my college days as a Psych major in experimental design, controls, population sampling and statistical analysis of results. I guess that is from where my attention to the small details comes. About five years back I discovered Google Scholar and I have been reading papers and abstracts ever since. I have close to 200 bookmarked most of which relate to cycling related issues and the effects/toxicity of ammonia, nitrite and nitrate on fish, inverts and aquatic plants.

I feel that the best way to have healthy fish and tanks is to have as much knowledge as possible about those things that we cannot see in tanks but which form the basis for the ecosystem in any tank.

What makes Planet Cat such a great site is the presence of scientists who are also fish keepers and who are willing to post and to respond to hobbyists like me. The same applies to the people who speak at fish events and whose brains I can pick for a bit. To all of you who are willing to spend time answering questions from hobbyists I would like to offer a big THANK YOU

And now, I return you back to the regularly scheduled Panaque discussion.........
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Re: Nitrogen fixing bacteria in the gut of Panaque nigrolineatus

Post by bekateen »

Matthew wrote:
Matthew, I'd say the same thing to you that I said to TTA; you know what you're talking about. You don't need to feel intimidated to join into any conversation with others just because they have various degrees behind their names. Moreover, even when you don't know what you're talking about, the best way to learn is by asking questions. Heck, if you look back at my start here, I asked plenty of questions and said plenty of dumb things, and I plan on... no, I expect to... keep doing so for a long time to come. :-
TTA wrote:
TTA, although this is getting off topic, our appreciation of gut microbes is changing pretty rapidly. Even in humans, the recognition of how beneficial gut microbes can be is reflected in the economic growth of "probiotics" as nutritional supplements. And, if you can tolerate me presenting a somewhat gross, but simultaneously funny (in my opinion) offshoot of this topic, here's where the field has been heading lately: Doctors are performing fecal transplants between people to help individuals with severe cases of antibiotic-resistant bacterial intestinal infections... Yes, it's exactly what it sounds like... And of course, drug companies are all over this - the FDA is considering defining some samples of feces as a "drug" which can be patented and sold. For more info, see this, this, this, this. There are actually DIY videos on YouTube for performing your own fecal transplant (e.g., here).

Cheers, Eric
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Re: Nitrogen fixing bacteria in the gut of Panaque nigrolineatus

Post by mcdonal1 »

Hi All,

My name is Ryan McDonald and I am the first author on the paper Nitrogenase diversity and activity in the gastrointestinal tract of the wood-eating catfish Panaque nigrolineatus. It makes me very happy to see there is such an extensive community who shares my interest in these organisms. I would be happy to answer any questions you may have.

Thanks.
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Re: Nitrogen fixing bacteria in the gut of Panaque nigrolineatus

Post by bekateen »

Hi Ryan,

Thank you so much for joining our discussion, and welcome to PlanetCatfish! :-)

I am not an authority on panaque taxonomy, so I'll leave that issue for other people to address. In the mean time, I have three questions for you:
  1. What do you know about the auxiliary lobe of the digestive tract in these animals?
  2. Do you have any specific ideas or evidence about what particular nutritional benefit these panaques might obtain from the N-fixing bacteria? In your paper, you seemed to be saying that the primary benefit might be to provide essential amino acids and organic micronutrients (vitamins, etc) rather than caloric macronutrients.
  3. Do you have any expectations as to how shifting these fish from a wood diet to an algae diet (or vice versa) would affect the bacterial diversity in the guts of these fish?
Again, thank you for offering input here.

Cheers, Eric
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Re: Nitrogen fixing bacteria in the gut of Panaque nigrolineatus

Post by matthewfaulkner »

Ryan,

Just like Eric said, thank you joining this discussion!

Could you shed some light on the origin and identity of the Panaque that you used?
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Re: Nitrogen fixing bacteria in the gut of Panaque nigrolineatus

Post by mcdonal1 »

Thanks for the great questions. I will answer them as best as I can.

1. The auxiliary lobe (AL) is a very interesting structure. It is small, bilobed, structure that straddles the midgut at the point where the intestines reverses its coiling direction. Structurally it resembles liver tissue (was previously referred to as the liver-like organ) but there is no known function. However, there is some anecdotal evidence to suggest is it involved in digesta processing. When fed algae wafer,s the feces in the foregut (prior to passing the AL) are a green slurry. However, immediately distal to the AL the digesta turns an almost white color and adopts a chalk-like consistency.
It is still not clear whether the AL contributes significantly to wood digestion. I have previously characterized the microbial community of the AL and found that was very similar to that of that of the surrounding tissue. There were some putative cellulose degrading and nitrogen fixing species identified. However, microscopic analysis of the AL did not identify any obvious structures used to house a symbiotic microbial community (perhaps akin to the shipworm gland of Deshayes or the bacterial pouch of Tetraponera ants).
2. Mature, structural wood is rich in carbohydrates but is extremely nitrogen deficient. The carbon to nitrogen ration of wood is much greater than that of the primary consumer. As such, organisms like termites, shipworms, or any other xylophagic systems need to supplement their diets with alternative nitrogen sources. Every xylophagic system described to date accomplishes this by harboring an extensive diazotrophic (nitrogen-fixing) microbial community which converts atmospheric dinitrogen to ammonia. This process is carried out exclusively by microorganisms and cannot be performed by the catfish. Having read some of the comments in the thread I remember one poster commenting about how ammonia is a fish waste product that is rapidly excreted. This is true, however, the ammonia that is generated by bacteria is not made available to the fish. The process of converting nitrogen gas to ammonia is extremely energy intensive (you are breaking a triple bond). To convert one molecule of atmospheric nitrogen to ammonia requires approximately 16 ATP. As such, the bacteria will not simply release this expensive metabolite into the environment. They very efficiently combine the ammonia with glutamate to form glutamine which is used in a variety of biosynthetic pathways. The nitrogen-containing compounds that made available to the fish will be either secondary metabolites or cellular components of dead/digested bacteria. If p. nigrolineatus is truly xylivorous, the vast majority of nitrogen-containing compounds found in every cell must be the product of biological nitrogen fixation.
The majority of the calories made available to the fish come from the sequential saccharification and fermentation of the structural polysaccharides in plant cell walls. The major component of wood is cellulose which is simply repeating glucose units joined by beta glycosidic linkages. The bacteria in the gut hydrolyze these linkages to release glucose which is used as an energy source by the microorganisms. Since the GI tract is anaerobic, the glucose is fermented to a variety of short chain fatty acids (butyric acid, propionic acid, etc..) which are taken up by the fish through their intestinal epithelium.
3. This is still an area of ongoing research but I certainly believe shifting the diet of P. nigrolineatus will result in a shift in the enteric microbiome. There are a few major factors that influence enteric microbial communities. First is environment (what microorganisms you are exposed to regularly). Second is host genetics. An organism’s immune system is a major force in shaping their microbiome. Third is diet. An organism’s diet ultimately determines what nutrients are available to the enteric microbial community. If an organisms consumes primarily plant material, there will be very little protein or fats available. As such, you would expect organisms capable of efficient polysaccharide hydrolysis and fermentation to out compete other organisms. Conversely, a carnivorous diet might select for a community that had a high capacity for lipid metabolism and proteolysis. Although there are many studies that have shown that diet affects the microbiome, it is still difficult to predict what the resulting community profile will look like.
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Re: Nitrogen fixing bacteria in the gut of Panaque nigrolineatus

Post by bekateen »

Thank you, Ryan. Those are very helpful answers.

I'm thinking about what you wrote in the context of other stories (referenced earlier in this thread) which observed weight loss in these panaques when fed a wood-only diet. If the species identification is correct, these fish are natural wood eaters and not primarily algae eaters. Considering this, then fish in captivity which get fed an algae-only or algae- and wood-diet are probably getting a nutrient-rich diet, relative to what they get in nature. And if we work on the assumption that fish in nature are at least satisfactorily nourished (since they are growing and reproducing), then this would mean fish in captivity should experience greater than normal body growth on the algae diet. As a result, if we then put them on a wood-only diet, I can imagine that there would be a natural metabolic contraction, with an associated weight-loss, or at least serious slowing of growth rate, on this nutrient-limiting diet. This would create the appearance, in the data, that that these fish are not adapted to survive exclusively on a wood-only diet; but it might simply be that their bodies are realigning with a more natural, balanced metabolism and growth rate. Is this consistent with your view about these fish?

By the way, is there any significance to the fact that the coil of the gut changes direction part-way along it's length? Why not continue to coil in one direction? Do you suppose this is creating some kind of counter-current exchange mechanism? I wouldn't think so, since I imagine that (A) the reversed tubes are not anatomically juxtaposed to the earlier segments of the gut, and (B) the walls of the gut are too think to operate as such an exchanger. But honestly, I can't think of any other explanation in nature that fits for such a counter-current organization.

Personally, I think that one of the more perspective-reorienting aspects of this work is that we need to stop limiting ourselves to the idea that herbivorous and xylivorous vertebrates must have large fermentation chambers in their guts, like the stomach of a cow or the cecum of a rabbit (which are both endotherms, whereas panaques are not; so the metabolic demands of panaques are much lower than those of cows and rabbits). And even if it seems to us like this system in the panaques is inadequate for providing the high quantities of caloric and nitrogen-rich nutrients that we expect panaques need, the fact of the matter is... (as I tell my students so often in cases like this)...the fact of the matter is that in nature, these fish represent a successful adaptation to the particular ecosystems where they're found; therefore, no matter how "insufficient their system appears" to be, the reality is that it is "sufficient enough" for the panaques.

Cheers, Eric
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Re: Nitrogen fixing bacteria in the gut of Panaque nigrolineatus

Post by Bas Pels »

Thanks for the above, Ryan.

You did explain why a wood eater would need nitrogen binding, and why this would not result in the excretion of harmful substances.

Still, I wonder the nitrogen binding takes place in the gut. That is, after the food-mass has passed the stomach, which is (at least in mammals) the place where most of the protein downgrading takes place. Bacteria living in the gut will never enter the stomach – therefore I wonder where these bacteria will be processed.

Rabbits eat their own faeces in order to benefit from the bacteria in their gut – but as far as anyone knows, Panaque do not, and I don’t think their mouths are capable of doing this.

Obviously it could be Panaque has changed the order of processing – for a wood eater, having a stomach in the traditional sense (a place to digest protein) will not make sense – and having the right kind of protein in the last part of the gut would certainly make sense – but that would imply these proteins would have to be found.

Perhaps these are even very interesting – most likely the Panaque gut will never become as acidic as a stomach does – if it did, anatomical evidence (the special lining) would most likely been found.
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