Ultrastructural Observations on Renal Schizogony of Leucocytozoon dubreuili in the American Robin

Abstract

The schizogonic development of Leucocytozoon dubreuili in the kidney proximal tubule cells of the American robin, Turdus migratorius, was studied by electron microscopy. Renal schizogony is initiated by the entry of certain hepatic merozoites into cells of the proximal tubules. Development of the schizont consists of coordinated sequence of events including extensive mitotic nuclear division, multiplication of mitochondria, increase in endoplasmic reticulum and ribosomes, differentiation of membranes, microtubules, micronemes and rhoptries, and cytoplasmic segmentation (cytomere formation). Merozoites form by budding around numerous centers in the schizont and, when mature, are bounded by a single plasma membrane subtended by microtubules. Each merozoite contains a large nucleus, a mitochondrion, and well developed apical complex consisting of 3 polar rings, paired rhoptries, and numerous micronemes. An atypical nuclear division observed in some maturing schizonts was characterized by the multiple fission of a nucleus within a persistent outer nuclear membrane and the absence of mitotic spindle apparatus. Alterations in infected renal cells consisted of disorganization and loss of cytoplasmic organelles and the accumulation of lipofuscin-like inclusions.

A citizen science-based survey of avian mortality focusing on haemosporidian infections in wild passerine birds

“…In addition to blood stages, CISH revealed parasite tissue stages in some birds, contributing new data on the exo-erythrocytic development of Haemoproteus and Leucocytozoon lineages in passerines. In hawfinches, Leucocytozoon meronts were exclusively found in the kidneys, suggesting this organ to be a common site of exo-erythrocytic development of the detected lineages, consistent with descriptions of renal merogony in other passeriform-specific Leucocytozoon [ 51 , 75 – 77 ]. In the hawfinch co-infected with two Leucocytozoon lineages (HAWF7 and COCCO01), multiple meronts were distributed across the renal parenchyma and seemed to develop primarily in epithelial cells of tubules, sometimes leading to expansion of the infected cells, occupying most of the tubular lumen.…”

Insights into the Biology of Leucocytozoon Species (Haemosporida, Leucocytozoidae): Why Is There Slow Research Progress on Agents of Leucocytozoonosis?

“…For example, some species of Parahaemoproteus and L. caulleryi produce elongated merozoites in the first generation of their exo-erythrocytic meronts [ 185 , 186 ], whereas this is not the case among Leucocytozoon species [ 3 ]. The presence of a pellicle in the elongate merozoites of L. caulleryi is similar to the ultrastructure of merozoites of other Haemoproteus and Plasmodium species, but is different from the merozoites of Leucocytozoon species, which do not contain a pellicle [ 4 , 175 ]. In addition, both H. mansoni and L. caulleryi parasitize galliform birds and are transmitted by Culicoides spp.…”

“…Such a close association indicates that the host cell is not simply a source of food for the parasite, as is the case with erythrocytes infected with malaria parasites, but rather that the parasite actively transforms the metabolism of the infected cells, turning them into a sort of “factory” producing material for parasite growth. This process is particularly pronounced during the development of megalomeronts, which cause a remarkable increase in the amount of chromatin and endoplasmic reticulum, as well as the number of mitochondria and other cellular structures in infected host cells [ 86 , 87 , 89 , 175 ]. Mitochondria have been observed within indentations of the nuclear envelope of gametocytes [ 176 , 177 ].…”

“…Fourth, unlike species of Plasmodium and Haemoproteus , merozoites of Leucocytozoon parasites lack a pellicle, making gametocytes fragile and easily deformed in blood films [ 4 , 175 ]. Deformed gametocytes usually predominate in blood films, making the detection of non-deformed host-parasite complexes and species identification difficult.…”

Exo-erythrocytic development of avian malaria and related haemosporidian parasites

“…4a, b), and only subsequent generations of meronts appear in other organs and cells. In L. dubreuili and L. fringillinarum , sporozoites initiate development of meronts in liver, but also in kidneys where they locate in renal tubular cells [177–180]. As meronts grow, nuclei of the host cells increase in size and the cytoplasm breaks down into numerous cytomeres, in which nuclear fission continues (Fig.…”