Whole Genome Sequencing and Comparative Genome Analysis of the Halotolerant Deep Sea Black Yeast Hortaea werneckii

Abstract

Hortaea werneckii, an extreme halotolerant black yeast in the order of Capnodiales, was recently isolated from different stations and depths in the Mediterranean Sea, where it was shown to be the dominant fungal species. In order to explore the genome characteristics of these Mediterranean isolates, we carried out a de-novo sequencing of the genome of one strain isolated at a depth of 3400 m (MC873) and a re-sequencing of one strain taken from a depth of 2500 m (MC848), whose genome was previously sequenced but was highly fragmented. A comparative phylogenomic analysis with other published H. werneckii genomes was also carried out to investigate the evolution of the strains from the deep sea in this environment. A high level of genome completeness was obtained for both genomes, for which genome duplication and an extensive level of heterozygosity (~4.6%) were observed, supporting the recent hypothesis that a genome duplication caused by intraspecific hybridization occurred in most H. werneckii strains. Phylogenetic analyses showed environmental and/or geographical specificity, suggesting a possible evolutionary adaptation of marine H. werneckii strains to the deep sea environment. We release high-quality genome assemblies from marine H. werneckii strains, which provides additional data for further genomics analysis, including niche adaptation, fitness and evolution studies.

Ecology and Evolution of Marine Fungi With Their Adaptation to Climate Change

“…The potential of some fungi for their phenotypic and genetic adaptation in response to extreme habitat and climate change has been acknowledged here. Several fungi have characterized themselves to adapt in environments with low water activity and high concentrations of toxic ions by complex molecular and cellular adaptation (Gostinèar et al, 2011;Gladfelter et al, 2019;Romeo et al, 2020). Spores of some marine fungi have developed strategies of sheath and appendages to attach, float, and adapt to a new environment.…”

“…These adaptation mechanisms and their effects are highly dependent on different levels of biological organization and follow a cascade of events (molecular and cellular, whole organisms, population, and community). Fungi isolated from hypersaline marine environments, deepsea hydrothermal vents, and deep-sea sediments have different molecular and cellular mechanisms for adaptation, e.g., gene expression, high osmolarity glycerol (HOG) signaling pathway, melanization of the cell wall, composition and accumulation of ions, enzymes involved in fatty acid modifications, and plasma membrane composition (Turk and Plemenitaš, 2002;Kogej et al, 2006;Romeo et al, 2020). Fungi with these characters have been described for genera such as Aspergillus, Cladosporium, Emericella, Eurotium, Hortaea, Trimmatostroma, and Wallemia.…”

“…Here we have discussed what molecular and cellular mechanisms determine the adaptation of Hortaea werneckii to marine habitat and how H. werneckii deals with climatic stressors such as high salinity (3-4.5 M) and temperature (Kejžar et al, 2015;Gunde-Cimerman et al, 2018;Romeo et al, 2020;Selbmann et al, 2020). Also, we have addressed the adaptations of Aspergillus terreus to the extreme conditions of a hydrothermal vent (Pang et al, 2020).…”

“…survival and adaptation tool in hypersaline, marine, and deep-sea environments (Plemenitaš et al, 2014;Gunde-Cimerman et al, 2018;Romeo et al, 2020).…”

The Mycobiota of the Deep Sea: What Omics Can Offer

“…In deep-sea hypersaline basins (salinity between 70 and 172 ppt) located in the Eastern Mediterranean Sea that harbored Ascomycota and Basidiomycota [ 85 ], a metatranscriptomic analysis revealed that the majority of the detected rRNA signatures were related to the genera Aspergillus and Penicillium [ 33 ]. The genus Hortaea is commonly detected from deep-sea environments [ 22 , 60 , 61 , 66 , 83 , 86 , 87 ], specifically the species H. werneckii , a black yeast that has been classified as halotolerant in Mediterranean deep-sea waters [ 88 ] and as halophilic in deep-sea hydrothermal vents [ 83 ]. Marine-derived Penicillium and Aspergillus species are an excellent and widely used source for many useful bioactive secondary metabolites [ 89 , 90 ].…”