Insights into eukaryogenesis from the fossil record

Abstract

Eukaryogenesis—the process by which the eukaryotic cell emerged—has long puzzled scientists. It has been assumed that the fossil record has little to say about this process, in part because important characters such as the nucleus and mitochondria are rarely preserved, and in part because the prevailing model of early eukaryotes implies that eukaryogenesis occurred before the appearance of the first eukaryotes recognized in the fossil record. Here, I propose a different scenario for early eukaryote evolution than is widely assumed. Rather than crown group eukaryotes originating in the late Paleoproterozoic and remaining ecologically minor components for more than half a billion years in a prokaryote-dominated world, I argue for a late Mesoproterozoic origin of the eukaryotic crown group, implying that eukaryogenesis can be studied using the fossil record. I review the proxy records of four crown group characters: the capacity to form cysts as evidenced by the presence of excystment structures; a complex cytoskeleton as evidenced by spines or pylomes; sterol synthesis as evidenced by steranes; and aerobic respiration—and therefore mitochondria—as evidenced by eukaryotes living in oxic environments, and argue that it might be possible to use these proxy records to infer the order in which these characters evolved. The records indicate that both cyst formation and a complex cytoskeleton appeared by late Paleoproterozoic time, and sterol synthesis appeared in the late Mesoproterozioc or early Neoproterozoic. The origin of aerobic respiration cannot as easily be pinned down, but current evidence permits the possibility that it evolved sometime in the Mesoproterozoic.

The origin of phagocytosis in Earth history

“…Likewise, the oldest eukaryotic steranes date to ca 820 to 720 Ma [60]. A conservative reading of these combined records (biomarker, fossil, and molecular) might suggest an origin of LECA after 1.2 Ga or so [129,131], with all older total-group eukaryotic fossils necessarily belonging to eukaryotic stem-lineages [48]. Overall, we could then put the origin of LECA into two camps or possibilities: 'LECAearly' (ca 1.8-1.6 Ga) and 'LECA-late' (less than 1.2 Ga)-or alternatively 'old LECA' and 'young LECA' [49] (figure 1 and table 1).…”

Evolution of a key enzyme of aerobic metabolism reveals Proterozoic functional subunit duplication events and an ancient origin of animals

“…Although our results may support a deep Paleoproterozoic origin of eukaryotes with a late Mesoproterozoic origin of the crown group, they do not support a late emergence of aerobic respiration (ca. 800 Ma; as suggested by Porter et al 34 ).…”

“…Some differences can be attributed to the use of the fossil Bangiomorpha pubescens —a presumed bangiophyte red alga—as a calibration point. Time estimates obtained without employing B. pubescens as a calibration point are 200–300 Ma younger than those that do 34 . Recently, the development of refined molecular clock methodologies has helped to reduce the disparities among molecular dating and the fossil evidence used to estimate clade age minima 26 , 35 .…”

“…Using molecular clock estimates of protein folds, the emergence of eukaryotes in the Paleoproterozoic is also corroborated 63 , 64 . Nevertheless, recent evidence suggest a late Mesoproterozoic origin of the eukaryotic crown group based mainly on eukaryotic sterols, which are presumed to have been present in the eukaryotic crown-ancestor and is absent from rock records until the early Neoproterozoic 34 . Although our results may support a deep Paleoproterozoic origin of eukaryotes with a late Mesoproterozoic origin of the crown group, they do not support a late emergence of aerobic respiration (ca.…”

The origin and rise of complex life: progress requires interdisciplinary integration and hypothesis testing

“…Porter [46] presents a barn-burning reinterpretation of the timing and tempo of eukaryogenesis, the process by which the key characteristics of modern eukaryotic cells were assembled over time, from their archaeal and alpha-proteobacterial antecedents, through to the last common ancestor of all living eukaryotes. The contemporary view is of stem and crown eukaryotes emerging early in the Proterozoic, existing at low diversity and perhaps in restricted environments or ecologies until a late Mesoproterozoic diversification of crown-eukaryotes.…”