Adaptive melanin response of the soil fungus Aspergillus niger to UV radiation stress at "Evolution Canyon", Mount Carmel, Israel

Abstract

Background: Adaptation is an evolutionary process in which traits in a population are tailored by natural selection to better meet the challenges presented by the local environment. The major discussion relating to natural selection concerns the portraying of the cause and effect relationship between a presumably adaptive trait and selection agents generating it. Therefore, it is necessary to identify trait(s) that evolve in direct response to selection, enhancing the organism's fitness. "Evolution Canyon" (EC) in Israel mirrors a microcosmic evolutionary system across life and is ideal to study natural selection and local adaptation under sharply, microclimatically divergent environments. The south-facing, tropical, sunny and xeric "African" slope (AS) receives 200%-800% higher solar radiation than the north-facing, temperate, shady and mesic "European" slope (ES), 200 meters apart. Thus, solar ultraviolet radiation (UVR) is a major selection agent in EC influencing the organism-environment interaction. Melanin is a trait postulated to have evolved for UV-screening in microorganisms. Here we investigate the cause and effect relationship between differential UVR on the opposing slopes of EC and the conidial melanin concentration of the filamentous soil fungus Aspergillus niger. We test the working hypothesis that the AS strains exhibit higher melanin content than strains from the ES resulting in higher UV resistance.

Methodology/principal findings: We measured conidial melanin concentration of 80 strains from the EC using a spectrophotometer. The results indicated that mean conidial melanin concentration of AS strains were threefold higher than ES strains and the former resisted UVA irradiation better than the latter. Comparisons of melanin in the conidia of A. niger strains from sunny and shady microniches on the predominantly sunny AS and predominantly shady ES indicated that shady conditions on the AS have no influence on the selection on melanin; in contrast, the sunny strains from the ES displayed higher melanin concentrations.

Conclusions/significance: We conclude that melanin in A. niger is an adaptive trait against UVR generated by natural selection.

Figure 1. Melanin concentration in A. niger strains from “Evolution Canyon” I, Israel.

(A) Mean (n = 40; stations and habitats pooled)±SE of AS and ES. (B) Box plot showing means (n = 10; typed by line within the box plot) and variations from six stations. AS2a and AS2b denote strains from sunny and shady microniches, respectively, whereas ES6a and ES6b indicate strains from shady and sunny micro- niches, respectively (the usage of “a” and “b” for ES6 is opposite to AS2 and is based on the order of predominant (a) and minor (b) habitats on the aforementioned stations). Means separation in columns by the Duncan's multiple range test, 5% level.

Figure 2. Relative culturability of A. niger strains after 4 h exposure to UVA irradiation plotted against conidial melanin concentration.

Regression equations: linear for AS strains (open circles) y = 34.383x+68.414, R² = 0.9166, P<0.001), and logarithmic curve for ES strains (solid circles) y = 16.334Ln(x)+100.67 R² = 0.9187: p<0.001).

Figure 3. Relative culturability of A. niger strains after 4 h exposure to UVA irradiation plotted against conidial melanin concentration for AS (A) and ES strains (B) from sunny (yellow circles) and shady (solid black circles) microniches.

Figure 4. Evolution Canyon I (study system) Lower Nahal Oren, Mount Carmel, Israel, A. Aerial View, B. Cross section (Source: Science from Israel-LPPLtd).