An archaeal symbiont-host association from the deep terrestrial subsurface

Abstract

DPANN archaea have reduced metabolic capacities and are diverse and abundant in deep aquifer ecosystems, yet little is known about their interactions with other microorganisms that reside there. Here, we provide evidence for an archaeal host-symbiont association from a deep aquifer system at the Colorado Plateau (Utah, USA). The symbiont, Candidatus Huberiarchaeum crystalense, and its host, Ca. Altiarchaeum hamiconexum, show a highly significant co-occurrence pattern over 65 metagenome samples collected over six years. The physical association of the two organisms was confirmed with genome-informed fluorescence in situ hybridization depicting small cocci of Ca. H. crystalense attached to Ca. A. hamiconexum cells. Based on genomic information, Ca. H. crystalense potentially scavenges vitamins, sugars, nucleotides, and reduced redoxequivalents from its host and thus has a similar metabolism as Nanoarchaeum equitans. These results provide insight into host-symbiont interactions among members of two uncultivated archaeal phyla that thrive in a deep subsurface aquifer.Recently, subsurface fluids discharged by a cold, CO 2 -driven geyser at the Colorado Plateau, Utah (Crystal Geyser) revealed the presence of multiple novel archaeal organisms, including the first representative of the Candidatus phylum Huberarchaeota [8], which we show to be part of the

Lipid analysis of CO2-rich subsurface aquifers suggests an autotrophy-based deep biosphere with lysolipids enriched in CPR bacteria

“…Altiarchaeota in Crystal Geyser also have Ca. H. crystalense as a symbiotic partner [69], which could derive its lipids from the Altiarchaeota and was indicated to possess genes, whose products might be involved in lysis of Altiarchaeota cells [12]. In addition, longer turnover times of the chemically stable ether-bound lipids of archaea [66,67] compared with DNA could deteriorate correlations.…”

Undinarchaeota illuminate the evolution of DPANN archaea

“…The presence and absence patterns of genes involved in core metabolic pathways of Undinarchaeota MAGs shows similar trends as seen in DPANN Cluster 2 archaea further supporting the sisterhood of this clade ( Figure 4, Supplementary Tables 7-9,12 ). For instance, most DPANN Cluster 2 archaea lack genes involved in core metabolic pathways, such as the electron transport chain, carbon fixation other than the RuBisCO gene, as well as transport and motility genes ( Figure 3 ) 10,13–16,23,25,39,74 . While Undinarchaeota seem to have more complete pathways than many of the DPANN Cluster 2 representatives, they appear metabolically less flexible than several members of DPANN Cluster 1 ( Figure 3 ) 30,31,75,76 .…”

“…For instance, members of the DPANN Cluster 1 have more complete nucleoside and lipid biosynthesis pathways and include free-living organisms. In particular, representatives of the Altiarchaeota have been suggested to comprise autotrophic archaea that may use the Wood-Ljungdahl pathway for carbon fixation 24,25,30 and while this lineage includes symbionts, these do not seem to be obligate 77,78 . In fact, Altiarchaeota have recently been found to include members that likely serve as hosts for Huberarchaeota belonging to DPANN Cluster 2 25 .…”

“…Relative abundances (Ar) were normalized based on the total read counts, i.e. the maximum number of reads of all metagenomes (Nm) divided by the sample read count (Ns), multiplied by number of reads of that particular sample that mapped to the genome (r), and the average read length (l), divided by the genome size (g) (Ar=Nm/Ns * (r*l/g)) 25,79 . Proportionality was analyzed using the R package propR 79 based on normalized relative abundances, followed by the centered log-ratio transformation.…”

“…For instance, members of Nanoarchaeota are ectosymbionts of TACK archaea 15–20 , Micrarchaeota were found in co-culture with Thermoplasmates 21,22 and Nanohaloarchaeota are dependent on halobacterial hosts 23 . Furthermore, evidence from FISH and co-occurrence analyses have suggested that Huberarchaeota may be ectosymbionts of members of the Altiarchaeota 24,25 . Yet, for most DPANN representatives, the identity of their symbiotic partners remains unclear.…”