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

Probst, Alexander J.; Elling, Felix J.; Castelle, Cindy J.; Zhu, Qingzeng; Elvert, Marcus; Birarda, Giovanni; Holman, Hoi‐Ying N.; Lane, Katherine R.; Ladd, Bethany; Ryan, M. Cathryn; Woyke, Tanja; Hinrichs, Kai−Uwe; Banfield, Jillian F.

doi:10.1038/s41396-020-0624-4

Cited by 61 publications

(35 citation statements)

References 83 publications

(117 reference statements)

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“…Correlations of lipid and metagenome analyses suggested that Ca. H. crystalense has a very specific lipid different from its host [16], supporting the notion that lipid biosynthesis is indeed carried out by this archaeon. Hence, the cells must obtain ferredoxin in a reduced state.…”

supporting

confidence: 55%

“…S1. (167,168,171,174) amino acids (71, 110-117, 120-128, 130-141, 144-166, 175-178) G1P (precursor for activated sugars) (42)(43)(44)(45)(46)(47)(48)(49)(50) activated sugars (185-209, 97, 215) glycogen (193,185,214) molecular building blocks via acetyl-CoA (36-39) IPP (87-91), pyruvate (41), DHAP (42)(43)(44)(45)(46)(47) AdoCbl (179-184) NAD(P)H (10)(11)(12)(13)(14)(15)(16), FADH 2 (3)(4)(5)(6)(7)(8)(9) PLP (1) THF derivate (17,18,(20)(21)(22)(23)(24)(25) red. ferredoxin (18,216) NTPs (51-69, 71-77, 80, 82) dNTPs (69, 70, 77, 79, 81, 82) ATP GTP (83,220) energy demanding processes synthesis of activated sugar glycogen degrataion (210), synthesis of activated sugars (186, 192-194, 196, 198, 203, 205, 207, 215), transfer of glycosyl gropus (229) lipid biosynthesis…”

Section: Huberiarchaeum Crystelensementioning

confidence: 99%

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An archaeal symbiont-host association from the deep terrestrial subsurface

Schwank

Bornemann

Dombrowski

et al. 2018

Preprint

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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 has a similar metabolism as Nanoarchaeum equitans and potentially scavenges vitamins, sugars, nucleotides, and reduced redox-equivalents from its host. These results provide insight into host-symbiont interactions among members of two uncultivated archaeal phyla that thrive in a deep subsurface aquifer.The DPANN (Diapherotrites, Parvarchaeota, Aigarchaeota, Nanoarchaeota, Nanohaloarchaeota) [1] radiation is a proposed monophyletic group of diverse archaeal phyla whose organisms exhibit mainly reduced genomes with limited metabolic capacities [2]. While most of these archaea were suggested to live in symbiosis with other microorganisms, respective hosts were only described for Nanoarchaeota [3,4] and Micrarchaeota (ARMAN) symbionts [5][6][7]. However, no DPANN-host interaction has been described for representatives in aquifer systems, where these archaea are particularly abundant and very diverse [2].Recently, subsurface fluids discharged by a cold, CO2-driven geyser at the Colorado Plateau, Utah (Crystal Geyser) revealed the presence of multiple novel archaeal organisms,

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supporting

confidence: 55%

Section: Huberiarchaeum Crystelensementioning

confidence: 99%

An archaeal symbiont-host association from the deep terrestrial subsurface

Schwank

Bornemann

Dombrowski

et al. 2018

Preprint

Self Cite

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“…Although the complete lipid profile of Ca. H. crystalense is unknown, correlations of lipid and metagenome analyses suggested that the organism carries at least one very specific lipid different from its host [16], supporting the notion that lipid biosynthesis is indeed carried out by this archaeon. Hence, the cells must obtain ferredoxin in a reduced state.…”

Section: Introductionmentioning

confidence: 79%

An archaeal symbiont-host association from the deep terrestrial subsurface

et al. 2019

Self Cite

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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

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“…Hemolysin has also been found in Saccharibacteria (formerly candidate phylum TM7), the only CPR phylum for which an epibiotic parasitic lifestyle has been demonstrated so far 12,13 . Recent coupled lipidomic-metagenomic analyses have shown that CPR bacteria that lack complete lipid biosynthesis are able to recycle membrane lipid from other bacteria 27 . In Vampirococcus , also devoid of phospholipid synthesis, a phospholipase gene (Vamp_34_196) predicted to be secreted and that has homologs involved in host phospholipid degradation in several parasitic bacteria 28 , may not only help disrupting the host membrane but also to generate a local source of host phospholipids that it can use to build its own cell membrane.…”

Section: Resultsmentioning

confidence: 99%

Reductive evolution and unique infection and feeding mode in the CPR predatory bacteriumVampirococcus lugosii

Moreira

Zivanovic

López-Archilla

et al. 2020

Preprint

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The Candidate Phyla Radiation (CPR) constitutes a large supergroup of mostly uncultured bacterial lineages discovered through metabarcoding and metagenomics in diverse environments. Having small cell sizes, reduced genomes, and limited biosynthetic capabilities, they are thought to be symbionts of other organisms from which they obtain essential biomolecules. However, the nature of this symbiosis (mutualistic, neutral, or parasitic) has been ascertained only for rare cultured members of the CPR phylum Saccharibacteria, which are epibiotic parasites of other bacteria. Here, we characterize the biology and the genome of Vampirococcus lugosii, which becomes the first described species of Vampirococcus, a genus of epibiotic bacteria morphologically identified decades ago. Vampirococcus belongs to the CPR phylum Absconditabacteria. It feeds on anoxygenic photosynthetic gammaproteobacteria, fully absorbing their cytoplasmic content. The cells divide epibiotically, forming multicellular stalks whose apical cells can more easily reach new hosts. Vampirococcus genome is small (1.3 Mbp) and highly reduced in biosynthetic metabolism genes. However, it is enriched in genes related to an elaborate, fibrous cell surface likely involved in complex interactions with the host. Comparative genomic analyses show that gene loss has been continuous during Absconditabacteria, and generally most CPR bacteria, evolution. Nonetheless, gene loss was compensated by gene acquisition by horizontal gene transfer and evolution de novo. In Vampirococcus, these innovations include new CRISPR-Cas effectors and a novel electron transport chain. Our findings confirm parasitism as a widespread lifestyle of CPR bacteria, which probably play a previously neglected virus-like ecological role in ecosystems, controlling bacterial populations by a unique form of predation.

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

Cited by 61 publications

References 83 publications

An archaeal symbiont-host association from the deep terrestrial subsurface

An archaeal symbiont-host association from the deep terrestrial subsurface

An archaeal symbiont-host association from the deep terrestrial subsurface

Reductive evolution and unique infection and feeding mode in the CPR predatory bacteriumVampirococcus lugosii

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