Cytoskeletal architecture and its evolutionary significance in amoeboid eukaryotes and their mode of locomotion

Abstract

The cytoskeleton is the hallmark of eukaryotic evolution. The molecular and architectural aspects of the cytoskeleton have been playing a prominent role in our understanding of the origin and evolution of eukaryotes. In this study, we seek to investigate the cytoskeleton architecture and its evolutionary significance in understudied amoeboid lineages belonging to Amoebozoa. These amoebae primarily use cytoplasmic extensions supported by the cytoskeleton to perform important cellular processes such as movement and feeding. Amoeboid structure has important taxonomic significance, but, owing to techniques used, its potential significance in understanding diversity of the group has been seriously compromised, leading to an under-appreciation of its value. Here, we used immunocytochemistry and confocal microscopy to study the architecture of microtubules (MTs) and F-actin in diverse groups of amoebae. Our results demonstrate that all Amoebozoa examined are characterized by a complex cytoskeletal array, unlike what has been previously thought to exist. Our results not only conclusively demonstrate that all amoebozoans possess complex cytoplasmic MTs, but also provide, for the first time, a potential synapomorphy for the molecularly defined Amoebozoa clade. Based on this evidence, the last common ancestor of amoebozoans is hypothesized to have had a complex interwoven MT architecture limited within the granular cell body. We also generate several cytoskeleton characters related to MT and F-actin, which are found to be robust for defining groups in deep and shallow nodes of Amoebozoa.

Three New Freshwater Cochliopodium Species (Himatismenida, Amoebozoa) from the Southeastern United States

“…“crystal UK‐YT2” (fig. G and H, respectively, in Tekle and Williams ). This MTOC was present in most of the cells and was typically located near the center of the cell and the nucleus.…”

“…This study reaffirms that the microtubule organization is conserved in certain clades of Cochliopodium . In our phylogenetic analysis “crystal UK‐YT2” and “crystal‐like UK‐YT3” grouped with C. larifeili , which all have prominent MTOCs located near the center of the cell and typically near the nucleus (Tekle and Williams ). The only other Cochliopodium species that has a prominent MTOC similar to these three species is C. gallicum (Tekle and Williams ), a taxon with an ambiguous phylogenetic position.…”

“…In our phylogenetic analysis “crystal UK‐YT2” and “crystal‐like UK‐YT3” grouped with C. larifeili , which all have prominent MTOCs located near the center of the cell and typically near the nucleus (Tekle and Williams ). The only other Cochliopodium species that has a prominent MTOC similar to these three species is C. gallicum (Tekle and Williams ), a taxon with an ambiguous phylogenetic position. Cochliopodium gallicum branched at the base of the tree in this study but was previously reported to form a sister group relationship with C. larifeili (Tekle ).…”

“…The architecture of the cytoplasmic microtubules has previously been found to be useful character for grouping amoebae (Tekle and Williams ). This study reaffirms that the microtubule organization is conserved in certain clades of Cochliopodium .…”

“…Most other Cochliopodium spp. lack prominent MTOC including the new isolate "Marrs Spring UK-YT4" belonging to a clade containing C. actinophorum and C. arabianum, which all have dense microtubular networks (Tekle and Williams 2016). Table 1.…”