Cytochromes c in Archaea: distribution, maturation, cell architecture, and the special case of Ignicoccus hospitalis

Abstract

Cytochromes c (Cytc) are widespread electron transfer proteins and important enzymes in the global nitrogen and sulfur cycles. The distribution of Cytc in more than 300 archaeal proteomes deduced from sequence was analyzed with computational methods including pattern and similarity searches, secondary and tertiary structure prediction. Two hundred and fifty-eight predicted Cytc (with single, double, or multiple heme c attachment sites) were found in some but not all species of the Desulfurococcales, Thermoproteales, Archaeoglobales, Methanosarcinales, Halobacteriales, and in two single-cell genome sequences of the Thermoplasmatales, all of them Cren- or Euryarchaeota. Other archaeal phyla including the Thaumarchaeota are so far free of these proteins. The archaeal Cytc sequences were bundled into 54 clusters of mutual similarity, some of which were specific for Archaea while others had homologs in the Bacteria. The cytochrome c maturation system I (CCM) was the only one found. The highest number and variability of Cytc were present in those species with known or predicted metal oxidation and/or reduction capabilities. Paradoxical findings were made in the haloarchaea: several Cytc had been purified biochemically but corresponding proteins were not found in the proteomes. The results are discussed with emphasis on cell morphologies and envelopes and especially for double-membraned Archaea-like Ignicoccus hospitalis. A comparison is made with compartmentalized bacteria such as the Planctomycetes of the Anammox group with a focus on the putative localization and roles of the Cytc and other electron transport proteins.

Just So Stories about the Evolution of Apoptosis

“…Among the unique bacterial products recognized by these adapters was cytochrome c and the proteins needed for its maturation, present in bacteria and absent in many of the Archaea [53]. Here it may be important to note that, while a cytochrome c-like protein may have been present, the adapter in our story was specialized to recognize the mature form of cytochrome c, complete with heme.…”

“…Here it may be important to note that, while a cytochrome c-like protein may have been present, the adapter in our story was specialized to recognize the mature form of cytochrome c, complete with heme. Most Archaea lack the machinery to construct this holocytochrome c [53]. (As an aside, it is worth remembering that APAF1 in animals recognizes only holocytochrome c.)…”

Reverse Methanogenesis and Respiration in Methanotrophic Archaea

“…DIET is normally achieved using multiheme cytochrome c proteins (MHCs) and conductive pili (i.e., nanowires) which are mainly found in bacteria that donate electrons extracellularly, such as Geobacter and Shewanella species [108–114]. Indeed, ANME-2a from seep-sediment samples seem to transfer electrons directly using large MHCs [107], which were found in the metagenome of ANME-2a [107, 115]. ANME-1 and the associated bacterial partner also overexpressed genes for extracellular MHCs during AOM [116], which complements previous findings of transcription [41] and translation [40] of ANME-1 related MHC genes.…”

“…ANME-1 do not seem to have di-heme cytochromes (Table 2) [115]. PGF related domains (IPR026453 and IPR026371) were present in all ANME but PEF-CTERM (IPR017474) related domains were absent in ANME-1 (Table 2).…”

Archaea catalyze iron-dependent anaerobic oxidation of methane

“…The AAA in our enrichment culture encode numerous (41 species) multiheme c-type cytochromes (Table S1). This number is much higher than for methanogens, of which only Methanosarcinales encodes few multiheme cytochromes, but similar to M. nitroreducens (38 species) (5), the sulfate-dependent ANME-1 (11 species) (28), ANME-2a (16 species) (29,31), as well as the iron-reducing archaea Ferroglobus placidus (22 species) and Geoglobus (15 species) (32).…”