Biosystematic study of the order Trichiales (Myxomycetes, Amoebozoa) with ultrastructural and phylogenetic approaches

  1. García Cunchillos, Iván
Dirigida por:
  1. Carlos Lado Rodríguez Director/a

Universidad de defensa: Universidad Autónoma de Madrid

Fecha de defensa: 07 de julio de 2021

Tribunal:
  1. Enrique Lara Pandi Presidente/a
  2. Pedro Jiménez Mejías Secretario
  3. Raquel Pino Bodas Vocal

Tipo: Tesis

Resumen

Myxomycetes, sometimes referred to as Myxogastria or acellular slime molds, comprise one of the most diverse lineages within the supergroup Amoebozoa. Myxomycetes develop a complex life cycle, with multiple assimilative and motile stages and a final static phase producing macroscopic spore-bearing fruiting bodies. The morphological features of the fruiting bodies and their auxiliary structures, i.e., stalk, peridium, capillitium, and spores, drive their systematics. Within Myxomycetes, Trichiales stands out as one of the most morphologically diverse orders, characterized by bright-colored spores and variously ornamented capillitium. The introduction of DNA-based phylogenetic analyses has challenged Trichiales systematics and has recovered unexpected phylogenetic relationships yet with a limited taxa sampling. In this thesis, a biosystematics study of the order Trichiales is conducted, based on phylogenetic and ultrastructural approaches, considering the broad Trichiales diversity in the Neotropics, rarely included in previous studies. First, the myxomycetes inhabiting the highlands of the Peruvian Andes (3000–5000 m) are reported. Second, the diversity of the Trichiales nivicolous species in the austral Andes are studied with morphological and phylogenetic approaches. Last, ultrastructural features of the capillitium and spores in Trichiales are analyzed in a new phylogenetic scenario. The highlands of the Peruvian Andes showed a higher number of Trichiales species than the other, comparatively more arid, studied regions in the Peruvian Andes, the coastal desert and ‘lomas’ formations (0–1500 m), and the ‘cardonal’ (1500–3000 m). Remarkably, the species assemblage was distinct in each of these regions, and only a few species occurred in all three. However, more similitudes appeared considering the myxobiota inhabiting other arid sectors in the southern and central Andes (Argentina and Chile besides Peru), which shared multiple species while only a few of them were exclusive taxa for each country. The nivicolous Trichiales myxomycetes inhabiting the austral Andes showed higher diversity than expected and a distinct species assemblage compared to other nivicolous habitats worldwide. This region harbors several endemic taxa, such as the two new species described here, Hemitrichia crassifila and Perichaena patagonica. Thus, the austral Andes may constitute a biodiversity hotspot of the order Trichiales, at least concerning nivicolous species. Trichiales taxonomy relies on the different features of the capillitium, chiefly the solid or hollow nature of the filaments and their ornamentation, particularly the capillitium spiral ornamentation. The study of the capillitium ultrastructural features in Trichiales with transmission electron microscopy showed five discrete ultrastructural capillitium types and two subtypes. Only one capillitium type consisted of solid or nearly solid filaments, i.e., threads, while the four remaining types presented hollow filaments or tubules. Besides, a capillitium spiral ornamentation, as seen with scanning electron microscopy, occurred in different ultrastructural capillitium types, questioning the value of this character in Trichiales taxonomy. Spore walls in Trichiales, as seen with transmission electron microscopy, consists of two layers, an outer layer comprising the ornamental elements and an inner layer, sub-divided into two sections. As seen with scanning electron microscopy, the spore ornamentation can include verrucae, bacula, pila, muri, and cristae elements, the two latter forming reticulate and subreticulate patterns on the spore surface. Each ornamental element defines a spore ornamentation type in Trichiales, verrucate, baculate, pilate, simple reticulate, and cristate, respectively. Besides, we distinguish two subtypes within the cristate ornamentation, previously unrecognized, the cristate reticulate, forming an incomplete reticulum, and the cristate patched, imprinting a patched pattern. Within the genetic regions studied, both the 18S rRNA and mtSSU reported highly similar phylogenetic relationships; however, the EF1A recovered phylogenetic affinities only for specimens of the same species. On the contrary, COI sequences obtained before editing processes may distort the inferred phylogenetic relationships. The Trichiales phylogeny, inferred from the concatenation of the 18S rRNA, EF1A, and mtSSU datasets, recovered five clades and 11 subclades, comprising Trichiales species, plus two paraphyletic clades comprising the sister order Cribrariales (outgroup). Remarkably, the species Dianema depressum and D. subretisporum, always circumscribed under the order Trichiales, branched within Cribrariales yet with uncertain phylogenetic affinities. Species of the genus Dictydiaethalium constituted the subclade C1, the single genus in the family Dictydiaethaliaceae, standing out as the only Trichiales taxa developing pseudocapillitium. Besides, all species known to produce capillitium threads constituted a monophyletic subclade (C2). This subclade included the genera Dianema, Calomyxa, Prototrichia, plus the species Licea variabilis. However, the phylogenetic relationships recovered not such circumscriptions, and thus we combine all these genera into a single one, Prototrichia. Species developing hollow capillitium tubules constituted different phylogenetic clades. The family Arcyriaceae sensu lato encompassed two paraphyletic clades (D and E) and included the genus Hemitrichia sense stricto (subclade D2). We retain a sensu lato concept due to the paraphyletic genus Arcyria, firstly reported, and the lack of characters discerning between Arcyria sensu stricto (clade E) and Arcyria sensu lato (clade E plus subclade D1). Besides an ultrastructural capillitium type B, all these species present stalks, sometimes absent, filled with spore-like bodies. The monophyletic family Trichiaceae included clades F and G, in which the stalks, when present, are filled with refuse matter. Several ultrastructural capillitium types occurred within Trichiaceae. This family encompassed all species traditionally circumscribed within the genus Perichaena, which, in turn, split into three clades, the genera Ophiotheca (clade F), Gulielmina gen. nov. (G2), and Perichaena s. str. (G4). Besides, we modify the genus Oligonema to accommodate phylogenetic relationships among species with cristate patched spores (a monophyletic group in subclade G1). The uncertain phylogenetic affinities among some G subclades and the still lack of fundamental taxa precluded propose further taxonomic modifications concerning this family.