Aggregatilinea lenta gen. nov., sp. nov., a slow-growing, facultatively anaerobic bacterium isolated from subseafloor sediment, and proposal of the new order Aggregatilineales ord. nov. within the class Anaerolineae of the phylum Chloroflexi

Nakahara, Nozomi; Nobu, Masaru K.; Takaki, Yoshihiro; Miyazaki, Masaru; Tasumi, Eiji; Sakai, Sanae; Ogawara, Miyuki; Yoshida, Naoko; Tamaki, Hideyuki; Yamanaka, Yuko; Katayama, Arata; Yamaguchi, Takashi; Takai, Ken; Imachi, Hiroyuki

doi:10.1099/ijsem.0.003291

Cited by 37 publications

(39 citation statements)

References 53 publications

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“…DNA extraction and PCR mixture preparation were performed on a clean bench to reduce contamination. DNA extraction from culture samples was performed as described previously 44 . The concentration of extracted DNA was measured using a Quant-iT dsDNA High-Sensitivity Assay Kit (Life Technologies).…”

Section: Methodsmentioning

confidence: 99%

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Isolation of an archaeon at the prokaryote-eukaryote interface

Imachi

Nobu

Nakahara

et al. 2019

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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...

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Section: Methodsmentioning

confidence: 99%

“…DNA extraction was performed as described previously 44 . Mate-paired library with an average insert size of 3000 bp was constructed according to the manufacturer’s instructions with Nextera Mate Pair Library Preparation kit (Illumina).…”

Section: Methodsmentioning

confidence: 99%

Isolation of an archaeon at the prokaryote-eukaryote interface

Imachi

Nobu

Nakahara

et al. 2019

Preprint

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“…Phylogenetic trees were calculated using RAxML ( We recovered five genomes that were taxonomically classified by GTDB-Tk within a lineage of the Chloroflexota phylum currently annotated as order SBR1031 (Table 1, Figure 2). Other genomes previously assigned to this clade included those proposed as the class Candidatus Thermofonsia (Ward et al 2018a) along with an isolate for which the order Aggregatilineales was recently proposed (Nakahara et al 2019). Following the isolation and characterization of Aggregatilinea lenta (Nakahara et al 2019), and the clustering of these organisms into an orderlevel clade by GTDB-Tk, we propose the reassignment of the organisms previously described as "Candidatus Thermofonsia" into the order Aggregatilineales.…”

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confidence: 78%

“…Other genomes previously assigned to this clade included those proposed as the class Candidatus Thermofonsia (Ward et al 2018a) along with an isolate for which the order Aggregatilineales was recently proposed (Nakahara et al 2019). Following the isolation and characterization of Aggregatilinea lenta (Nakahara et al 2019), and the clustering of these organisms into an orderlevel clade by GTDB-Tk, we propose the reassignment of the organisms previously described as "Candidatus Thermofonsia" into the order Aggregatilineales. This order is primarily made up of nonphototrophic organisms but also contains some members with full suites of phototrophy genes, which appear to have been derived via horizontal gene transfer from members of the Chloroflexia class of Chloroflexota (Ward et al, 2018a).…”

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confidence: 78%

“…The environmental range exhibited by known members of the SBR1031/Aggregatilineales was previously somewhat limited. Previously recovered genomes of members of this group were sourced from hot spring environments (Ward et al, 2018a, Ward et al, 2019, with the single known isolate isolated from subseafloor sediments (Nakahara et al 2019). 16S rRNA sequences of SBR1031 have been recovered from more diverse environments including hot springs (Ward et al, 2017, Ward 2017), contaminated soils (Militon et al 2010), and wastewater (Björnsson et al 2002).…”

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Microbial mats in the Turks and Caicos Islands reveal diversity and evolution of phototrophy in the Chloroflexota order Aggregatilineales

Ward

Lingappa

Grotzinger

et al. 2020

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Genome-resolved metagenomic sequencing approaches have led to a substantial increase in the recognized diversity of microorganisms; this included the discovery of novel metabolic pathways in previously recognized clades, and has enabled a more accurate determination of the extant distribution of key metabolisms and how they evolved over Earth history. Here, we present metagenome-assembled genomes of members of the Chloroflexota (formerly Chloroflexi or Green Nonsulfur Bacteria) order Aggregatilineales (formerly SBR1031 or Thermofonsia) discovered from sequencing of thick and expansive microbial mats present in an intertidal lagoon on Little Ambergris Cay in the Turks and Caicos Islands. These taxa included multiple new lineages of Type 2 reaction center-containing phototrophs that were not closely related to previously described phototrophic Chloroflexota—revealing a rich and intricate history of horizontal gene transfer and the evolution of phototrophy and other core metabolic pathways within this widespread phylum.

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