Skin glands of an aquatic salamander vary in size and distribution and release antimicrobial secretions effective against chytrid fungal pathogens

Abstract

Amphibian skin is unique among vertebrate classes, containing a large number of multicellular exocrine glands that vary among species and have diverse functions. The secretions of skin glands contain a rich array of bioactive compounds including antimicrobial peptides (AMPs). Such compounds are important for amphibian innate immune responses and may protect some species from chytridiomycosis, a lethal skin disease caused by the fungal pathogens (Bd) and (Bsal). While the bioactivity of skin secretions against Bd has been assessed for many amphibian taxa, similar studies are lacking for Bsal, a chytrid fungus that is especially pathogenic for salamanders. We studied the skin glands and their potential functions in an aquatic salamander, the three-toed amphiuma (). Skin secretions of captive adult salamanders were analyzed by RP-HPLC and tested against the growth of Bd and Bsal using assays. We found that compounds within collected skin secretions were similar between male and female salamanders and inhibited the growth of Bd and Bsal. Thus, skin secretions that protect against Bd may also provide protection against Bsal. Histological examination of the skin glands of preserved salamanders revealed the presence of enlarged granular glands concentrated within caudal body regions. A site of potential gland specialization was identified at the tail base and may indicate specialized granular glands related to courtship and communication.

Skin defenses of North American salamanders against a deadly salamander fungus

“…Similar results were found for Bd . Considering that skin peptides from two other salamander species (tiger salamanders, A. tigrinum; and three‐toed amphiuma, Amphiuma tridactylum ) fully inhibited Bsal and/or Bd growth at concentrations between 75 and 750 μg mL −1 , it was unexpected that A. maculatum skin peptides did not also completely inhibit the growth of Bsal or Bd at even the highest concentration of 1000 μg mL −1 (Sheafor et al ., 2008; Pereira et al ., 2018). It was also unexpected that predictive index of resistance (PIR) values were not similar for both chytrid pathogens.…”

“…These results are contrary to our prediction that skin peptides would have similar effects on the growth of both chytrid pathogens. Only three previous studies have compared Bsal and Bd responses to amphibian skin peptides (Pereira et al ., 2018; Smith et al ., 2018; Woodhams et al ., 2020). Skin peptides from fire salamanders ( Salamandra salamandra ) and Sierra Nevada yellow‐legged frogs ( Lithobates [= Rana ] sierrae ) inhibited the growth of both chytrid pathogens similarly (Smith et al ., 2018; Woodhams et al ., 2020).…”

“…(2006b) and Pereira et al . (2018) . Salamanders were individually submerged in collection buffer (CB, 50 mmol 1 −1 sodium chloride, 25 mmol 1 −1 sodium acetate, pH 7) within a plastic bag or bin.…”

An insight into the skin glands, dermal scales and secretions of the caecilian amphibian Ichthyophis beddomei

“…Amphibian skin is an exocrine organ that produces skin secretion, which contributes to several aspects of biology, especially homeostasis, cutaneous respiration, conspecific communication, offence and defence ( Fox, 1986 , Duellman and Trueb, 1986 ). These roles are generally assigned to the wide variety of bio-active molecules that are present in the skin gland secretions ( Zasloff, 1987 , Zasloff, 2002 , Erspamer, 1994 , Fredericks and Dankert, 2000 , Gomes et al, 2007 , Pereira et al, 2018 , Siano et al, 2018 ). Several bioactive peptides, amines ( Erspamer, 1994 ) and over 800 alkaloids have been reported from anurans and salamanders ( Daly et al, 2005 ).…”

Investigating the potential use of an ionic liquid (1-Butyl-1-methylpyrrolidinium bis(trifluoromethylsulfonyl)imide) as an anti-fungal treatment against the amphibian chytrid fungus, Batrachochytrium dendrobatidis

“…There are active amphibian conservation projects to mitigate chytrid impacts on amphibian populations using habitat management [18], amphibian translocations [19,20], amphibian reintroductions [21], and amphibian capture-treat-release [22]. Other research has searched for cures of infected individuals, including but not limited to probiotics/microbiomes [13,[23][24][25][26][27][28]; antimicrobial peptides [29][30][31][32][33]; anti-fungal baths and elevated body temperature [34][35][36]), or natural selection of resistance/tolerance genes (e.g., mycobiome [37]; MHC/immunogenes [38][39][40][41]).…”