Isolation of an archaeon at the prokaryote-eukaryote interface

Abstract

34The origin of eukaryotes remains enigmatic. Current data suggests that eukaryotes may 35 have risen from an archaeal lineage known as "Asgard archaea". Despite the eukaryote-36 like genomic features found in these archaea, the evolutionary transition from archaea to 37 eukaryotes remains unclear due to the lack of cultured representatives and corresponding 38 physiological insight. Here we report the decade-long isolation of a Lokiarchaeota-related 39Asgard archaeon from deep marine sediment. The archaeon, "Candidatus 40Prometheoarchaeum syntrophicum strain MK-D1", is an anaerobic, extremely slow-41 growing, small cocci (~550 nm), that degrades amino acids through syntrophy. Although 42 eukaryote-like intracellular complexities have been proposed for Asgard archaea, the 43 isolate has no visible organella-like structure. Ca. P. syntrophicum instead displays 44 morphological complexity -unique long, and often, branching protrusions. Based on 45 cultivation and genomics, we propose an "Entangle-Engulf-Enslave (E 3 ) model" for 46 eukaryogenesis through archaea-alphaproteobacteria symbiosis mediated by the physical 47 complexities and metabolic dependency of the hosting archaeon. 48 49 How did the first eukaryotic cell emerge? So far, among various competing evolutionary 50 models, the most widely accepted are the symbiogenetic models in which an archaeal 51 host cell and an alphaproteobacterial endosymbiont merged to become the first eukaryotic 52 cell 1-4 . Recent metagenomic discovery of Lokiarchaeota (and the Asgard archaea 53 superphylum) led to the theory that eukaryotes originated from an archaeon closely 54 related to Asgard archaea 5,6 . The Asgard archaea genomes encode a repertory of proteins 55 hitherto only found in Eukarya (eukaryotic signature proteins -ESPs), including those 56 involved in membrane trafficking, vesicle formation/transportation, ubiquitin and 57 cytoskeleton formation 6 . Subsequent metagenomic studies have suggested that Asgard 58 archaea have a wide variety of physiological properties, including hydrogen-dependent 59 anaerobic autotrophy 7 , peptide or short-chain hydrocarbon-dependent organotrophy 8-11 60 and rhodopsin-based phototrophy 12,13 . A recent study suggests that an ancient Asgard 61 archaea degraded organic substances and syntrophically handed off reducing equivalents 62 (e.g., hydrogen and electrons) to a bacterial partner, and further proposes a symbiogenetic 63 model for the origin of eukaryotes based on this interaction 14 . However, at present, no 64 single representative of the Asgard archaea has been cultivated and, thus, the physiology 65 and cell biology of this clade remains unclear. In an effort to close this knowledge gap, 66 3 we successfully isolated the first Asgard archaeon and here report the physiological 67 characteristics, potentially key insights into the evolution of eukaryotes. 68 69 Isolation of an Asgard archaeon 70Setting out to isolate uncultivated deep marine sediment microorganisms, we engineered 71 and operated a methane-fed continuous-fl...

Debating Eukaryogenesis—Part 1: Does Eukaryogenesis Presuppose Symbiosis Before Uptake?

“…In this light, the very recent, first successful cultivation of an Asgard archaeon, Prometheoarchaeum, (resembling the “hosts” involved in eukaryogenesis, [ 11–13 ] but not belonging to the group most related to the “host”) shows it to have extensions, demonstrating increased curvature and possibilities for membrane–membrane interactions. [ 14 ] Further research could show whether these archaea might occasionally take up their symbiotic partners. Even before this finding, some problems with the proposals based on full blown phagocytosis were obvious.…”

“…The recent cultivation of an Asgard representative without indications for endocytic mechanisms, but with membrane extensions makes the whole “parasite precursor for mitochondria” model less likely. [ 14 ]…”

“…[ 25 ] This conclusion was born out upon the cultivation of an Asgard representative mentioned above. [ 14 ] Finally, as the “Asgard” metagenomes seem to predict operational ETCs, even pinocytosis could disturb their membrane potential. Thus, endo/phagocytic models need to explain adequate ATP generation in the absence of adequately functioning ETCs.…”

“…[ 20 ] This seems to be in line with observations in the cultivated Asgard archaeon that lives in symbioses and has metabolic pathways that could be enhanced by transferring metabolites to bacteria capable of using molecular oxygen as the final electron‐acceptor. [ 14 ] The essence of symbiogenesis is nicely described by Nick Lane: “The dominant selective forces driving eukaryotic evolution arose from within the cell, not the external environment.” [ 3 ] However, I disagree when he downplays the role of O 2 by stressing that even after the GOE many environments were still anoxic (which is hardly relevant). Also the existence of anaerobic eukaryotes does not mean that these in anyway reflect what might have happened during evolution towards LECA or that LECA might have had mitochondria with anaerobic capabilities.…”

“…Whatever the details, such a merger is not unlikely to have occurred in the Asgard communities described in. [ 14 ]…”