Novel Hydrogenosomes in the Microaerophilic JakobidStygiella incarcerata

Abstract

Mitochondrion-related organelles (MROs) have arisen independently in a wide range of anaerobic protist lineages. Only a few of these organelles and their functions have been investigated in detail, and most of what is known about MROs comes from studies of parasitic organisms such as the parabasalid Trichomonas vaginalis. Here, we describe the MRO of a free-living anaerobic jakobid excavate, Stygiella incarcerata. We report an RNAseq-based reconstruction of S. incarcerata’s MRO proteome, with an associated biochemical map of the pathways predicted to be present in this organelle. The pyruvate metabolism and oxidative stress response pathways are strikingly similar to those found in the MROs of other anaerobic protists, such as Pygsuia and Trichomonas. This elegant example of convergent evolution is suggestive of an anaerobic biochemical ‘module’ of prokaryotic origins that has been laterally transferred among eukaryotes, enabling them to adapt rapidly to anaerobiosis. We also identified genes corresponding to a variety of mitochondrial processes not found in Trichomonas, including intermembrane space components of the mitochondrial protein import apparatus, and enzymes involved in amino acid metabolism and cardiolipin biosynthesis. In this respect, the MROs of S. incarcerata more closely resemble those of the much more distantly related free-living organisms Pygsuia biforma and Cantina marsupialis, likely reflecting these organisms’ shared lifestyle as free-living anaerobes.

Demystifying Eukaryote Lateral Gene Transfer (Response to Martin 2017 DOI: 10.1002/bies.201700115)

“…However, Martin specifically takes issue with our discussion of the origins of the pyruvate:ferredoxin oxidoreductase (PFO) and pyruvate:NADP+ oxidoreductase (PNO) enzymes that function in anaerobic ATP generation. He suggests that the interpretation in our paper is “that PFO entered the eukaryotic lineage via lateral acquisition long after mitochondria arose and was then distributed among diverse eukaryotic lineages via LGT.” This interpretation, Martin contends, ignores an alternative plausible scenario involving ancient duplications prior to LECA followed by massive numbers of parallel secondary losses in most eukaryote lineages. This is incorrect.…”

“…This is incorrect. In fact, we explicitly highlighted “the overall lack of resolution in these trees, and the lack of a clear prokaryotic sister group to eukaryotes that could point to these enzymes being either of mitochondrial origin, or laterally transferred from a specific prokaryotic group.” The paragraph from which this quote is taken clearly referred to PFO, as well as to [FeFe]‐hydrogenase. We further emphasized that it is unlikely that PFO, specifically, originated from an alphaproteobacterial (mitochondrial) source: it may therefore have been laterally acquired, or it may have been present in LECA, having originated from a different source.…”

Mitochondrial Genome Evolution and a Novel RNA Editing System in Deep-Branching Heteroloboseids

“…To the original dataset, we added sequences from the BB2 transcriptomic data, as well as from Pharyngomonas kirbyi transcriptome (data from Harding et al 2016; GECH01000000), plus six other Excavates: Spironucleus vortens, Tritrichomonas foetus, Diplonema papillatum, Leishmania major , “Seculamonas ecuadoriensis” , “Jakoba bahamensis” (all available in GenBank, http://www.ncbi.nlm.nih.gov/, last accessed February 10, 2016), and Stygiella incarcerata (Leger et al 2016). …”

Symbiogenesis, gradualism, and mitochondrial energy in eukaryote origin

“…Two main ideas are currently discussed for the origin of eukaryotic anaerobes, one gradualist, one symbiogenic. The gradualist view is that eukaryotes started out their evolutionary history as obligate aerobes, that the ancestral mitochondrion was an obligate aerobe specialist like Rickettsia (68), and that the ability to survive in anaerobic environments was gradually acquired during evolution in various eukaryotic lineages via lateral gene transfer (LGT), either from prokaryotes or from eukaryotes that had themselves become anaerobic via earlier gradual LGTs (69,70,71,72,73). There are several major problems with the origin of eukaryotic anaerobes via LGT, as discussed at length elsewhere (74), in addition to minor problems, such as the fact that the gradualist LGT origin for eukaryote anaerobes hinges wholly upon Lamarckian inheritance (traits being impressed from the environment into eukaryotic inheritance).…”

“…How can eukaryotes acquire genes from donors that lack the traits to be acquired? Third, the popularity of eukaryote LGT (69,70,71,72,140,144,145) should not obscure the fact that it is Lamarckian in tooth and claw. Eukaryote LGT proponents are saying that the genes required for survival in anaerobic environments (72), or the genes required for the origin of eukaryote complexity (141) are first acquired from outside the eukaryotic lineage, then inherited within eukaryotes to fulfill some purpose, for example adaptation to anaerobic environments or origins of complexity.…”