A histological atlas of the tissues and organs of neotenic and metamorphosed axolotl

Demircan, Turan; İlhan, Ayşe Elif; Aytürk, Nilüfer; Yıldırım, Berna; Öztürk, Gürkan; Keskin, İlknur

doi:10.1016/j.acthis.2016.07.006

Cited by 40 publications

(46 citation statements)

References 48 publications

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“…We observed that feeding behavior of the metamorphic axolotl change during metamorphosis, the animals tend to eat less often (low appetite), which might account for the decreased fecal diversity. Although no major restructuring of intestine via metamorphosis was apparent as described before 16 , we observed a higher number of goblet cells and thicker mucus layer in the metamorphic gut tissue compared to neotenic gut (Supplementary Fig. S9 ).…”

Section: Discussionsupporting

confidence: 55%

“…Natural accumulation (as in anurans) or administration (as in axolotl) of THs leads to critical reorganization of organs in order to adapt terrestrial life conditions. This adaptive process includes reconstruction or loss of some existing organs and extremities, and formation of new ones 15 , 16 . A prominent example of reconstruction is observed in digestive tract of tadpole.…”

Section: Introductionmentioning

confidence: 99%

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Experimentally induced metamorphosis in highly regenerative axolotl (ambystoma mexicanum) under constant diet restructures microbiota

Demircan

Ovezmyradov

Yıldırım

et al. 2018

Sci Rep

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Axolotl (Ambystoma mexicanum) is a critically endangered salamander species and a model organism for regenerative and developmental biology. Despite life-long neoteny in nature and in captive-bred colonies, metamorphosis of these animals can be experimentally induced by administering Thyroid hormones (THs). However, microbiological consequences of this experimental procedure, such as host microbiota response, remain largely unknown. Here, we systematically compared host bacterial microbiota associated with skin, stomach, gut tissues and fecal samples, between neotenic and metamorphic axolotls based on 16S rRNA gene sequences. Our results show that distinct bacterial communities inhabit individual organs of axolotl and undergo substantial restructuring through metamorphosis. Skin microbiota among others, shifted sharply, as highlighted by a major transition from Firmicutes-enriched to Proteobacteria-enriched relative abundance and precipitously decreased diversity. Fecal microbiota of neotenic and metamorphic axolotl shared relatively higher similarity, suggesting that diet continues to shape microbiota despite fundamental transformations in the host digestive organs. We also reproduced the previous finding on reduction in regenerative capacity in limbs of axolotl following metamorphosis, highlighting the need to investigate whether shifts in microbiota is causally linked to regenerative capacity of axolotl. The initial results on axolotl microbiota provide novel insights into microbiological aspects of axolotl metamorphosis and will establish a baseline for future in-depth studies.

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Section: Discussionsupporting

confidence: 55%

Section: Introductionmentioning

confidence: 99%

Experimentally induced metamorphosis in highly regenerative axolotl (ambystoma mexicanum) under constant diet restructures microbiota

Demircan

Ovezmyradov

Yıldırım

et al. 2018

Sci Rep

Self Cite

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“…We observed that feeding behavior of the metamorphic Axolotl change during metamorphosis, the animals tend to eat less often (low appetite), which might account for the decreased fecal diversity. Although no major restructuring of intestine via metamorphosis was apparent as described before 16 , we observed a higher number of goblet cells and thicker mucus layer in the metamorphic gut tissue compared to neotenic gut (Supplementary Fig. S8).…”

Section: Discussionsupporting

confidence: 55%

Experimentally Induced Metamorphosis in Axolotl (Ambystoma mexicanum) Under Constant Diet Restructures Microbiota Accompanied by Reduced Limb Regenerative Capacity

Demircan

Ovezmyradov

Yıldırım

et al. 2018

Preprint

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38Axolotl (Ambystoma mexicanum) is a critically endangered salamander species and a 39 model organism for regenerative and developmental biology. Despite life-long neoteny in 40 nature and in captive-bred colonies, metamorphosis of these animals can be 41 experimentally induced by administering Thyroid hormones (THs). However, biological 42 consequences of this experimental procedure, such as host microbiota response and 43 implications for regenerative capacity, remain largely unknown. Here, we systematically 44 compared host bacterial microbiota associated with skin, stomach, gut tissues and fecal 45 samples based on 16S rRNA gene sequences, along with limb regenerative capacity, 46 between neotenic and metamorphic Axolotls. Our results show that distinct bacterial 47 communities inhabit individual organs of Axolotl and undergo substantial restructuring 48 through metamorphosis. Drastic restructuring was observed for skin microbiota, 49 highlighted by a major transition from Firmicutes-enriched to Proteobacteria-enriched 50 relative abundance and precipitously decreased diversity. Remarkably, shifts in 51 microbiota was accompanied by a steep reduction in limb regenerative capacity. Fecal 52 microbiota of neotenic and metamorphic Axolotl shared relatively higher similarity, 53suggesting that diet continues to shape microbiota despite fundamental transformations in 54 the host digestive organs. The results provide novel insights into microbiological and 55 regenerative aspects of Axolotl metamorphosis and will establish a baseline for future in-56 depth studies. 57 58 59 60 61 62 63 Metazoan genomes have diversified and evolved in the presence of associated host 64 microbiota. The evolution of morphology and function of animal organ systems may have 65 been influenced by interactions with their microbial partners 1 . From the host perspective, 66 symbioses between metazoans and microbes provide a synergetic impact to operate 67 essential functions for normal growth, development and behavior 2-4 . Studies on host-68 microbiome interactions in health and disease conditions indicate that perturbation of the 69 crosstalk between the host and microorganisms may lead to deleterious consequences 70 such as developmental defects 3,5 , increased susceptibility to infectious diseases 6,7 and 71 ultimately fitness costs 8 . Even though host genotypes 9 and environmental factors, such 72 as diet and habitat 10,11 , were shown to strongly impact the composition and structure of 73 animal microbiota, ecological forces shaping assembly of the host associated microbial 74 communities have still been poorly understood. 75 76 Amphibians, which undergo dramatic morphological changes through metamorphosis, 77 exhibit explicitly altered biphasic life stages to tackle developmental challenges. 78 Remarkably, metamorphosis in several marine animal species such as sponges, corals, 79 crabs, sea urchins, an ascidians is mediated by bacterial community 12 . Thyroid hormones 80 (THs) are key players in initiation and completion of metamor...

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“…In A. mexicanum, the interatrial septum is formed during postembryonic development at stage 57 (subadult), but there is no evidence of valve formation between both chambers 67 , on the other hand only changes have been observed in the number and organization of cardiomyocytes in the ventricular zone, in such study authors focused in the ventricular zone and not in the atrial zone 21 . However, in metamorphic organisms such as A. tigrinum, after metamorphosis the main perfusion pathway is down to the entire length of the pulmonary artery that is located in the atrial zone 21 . The transcriptional profiles of the genes related to the morphogenesis of the atrial septum and the coronary vasculature suggest that this process begins during the SII of metamorphosis in A. velasci.…”

Section: Discussionmentioning

confidence: 94%

Multi-organ transcriptomic landscape ofAmbystoma velascimetamorphosis

Palacios-Martínez

Caballero-Pérez

Espinal-Centeno

et al. 2020

Preprint

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Metamorphosis is a postembryonic developmental process that involves morphophysiological and behavioral changes, allowing organisms to adapt into a novel environment. In some amphibians, aquatic organisms undergo metamorphosis to adapt in a terrestrial environment. These organisms experience major changes in their circulatory, respiratory, digestive, excretory and reproductive systems. We performed a transcriptional global analysis of heart, lung and gills during diverse stages of Ambystoma velasci metamorphosis. In our analyses, we identified eight gene clusters for each organ, according to the expression patterns of differentially expressed genes. We found 4,064 differentially expressed genes in the heart, 4,107 in the lung and 8,265 in the gills. Among the differentially expressed genes in the heart, we observed genes involved in the differentiation of cardiomyocytes in the interatrial zone, vasculogenesis and in the maturation of coronary vessels. In the lung, we found genes differentially expressed related to angiogenesis, alveolarization and synthesis of the surfactant protein. In the case of the gills, the most prominent biological processes identified are degradation of extracellular matrix, apoptosis and keratin production. Our study sheds light on the transcriptional responses and the pathways involved in the transformation of the facultative metamorphic salamander A. velasci in an organ-specific manner.

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A histological atlas of the tissues and organs of neotenic and metamorphosed axolotl

Cited by 40 publications

References 48 publications

Experimentally induced metamorphosis in highly regenerative axolotl (ambystoma mexicanum) under constant diet restructures microbiota

Experimentally induced metamorphosis in highly regenerative axolotl (ambystoma mexicanum) under constant diet restructures microbiota

Experimentally Induced Metamorphosis in Axolotl (Ambystoma mexicanum) Under Constant Diet Restructures Microbiota Accompanied by Reduced Limb Regenerative Capacity

Multi-organ transcriptomic landscape ofAmbystoma velascimetamorphosis

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