Unexpected host dependency of Antarctic Nanohaloarchaeota

Abstract

In hypersaline environments, Nanohaloarchaeota (Diapherotrites, Parvarchaeota, Aenigmarchaeota, Nanoarchaeota, Nanohaloarchaeota [DPANN] superphylum) are thought to be free-living microorganisms. We report cultivation of 2 strains of Antarctic Nanohaloarchaeota and show that they require the haloarchaeon Halorubrum lacusprofundi for growth. By performing growth using enrichments and fluorescence-activated cell sorting, we demonstrated successful cultivation of Candidatus Nanohaloarchaeum antarcticus, purification of Ca. Nha. antarcticus away from other species, and growth and verification of Ca. Nha. antarcticus with Hrr. lacusprofundi; these findings are analogous to those required for fulfilling Koch’s postulates. We use fluorescent in situ hybridization and transmission electron microscopy to assess cell structures and interactions; metagenomics to characterize enrichment taxa, generate metagenome assembled genomes, and interrogate Antarctic communities; and proteomics to assess metabolic pathways and speculate about the roles of certain proteins. Metagenome analysis indicates the presence of a single species, which is endemic to Antarctic hypersaline systems that support the growth of haloarchaea. The presence of unusually large proteins predicted to function in attachment and invasion of hosts plus the absence of key biosynthetic pathways (e.g., lipids) in metagenome assembled genomes of globally distributed Nanohaloarchaeota indicate that all members of the lineage have evolved as symbionts. Our work expands the range of archaeal symbiotic lifestyles and provides a genetically tractable model system for advancing understanding of the factors controlling microbial symbiotic relationships.

Differential polysaccharide utilization is the basis for a nanohaloarchaeon : haloarchaeon symbiosis

“…Nanoarchaeum antarcticus), and other microbial strains including heterotrophic haloarchaeon Halorubrum lacusprofundi , was published by Hamm et al . (2019) 25 . This exciting development supports the hypothesis of Andrade et al .…”

The evolutionary origins of extreme halophilic Archaeal lineages

“…The red (R) indicators represent the different placements proposed for the Nanohaloarchaea, while the purple (P) indicators are used for the Methanonatronarchaeia. Sources for each placement: R1 (Narasingarao et al, 2012) , R2 (Andrade et al, 2015) , R3 (Aouad et al, 2018); P1 (Sorokin et al, 2017) , and P2 (Aouad et al, 2019). be highly recombinogenic (Mohan et al, 2014;Naor et al, 2012) and are likely physically associated with at least some of the Nanohaloarchaea (Andrade et al, 2015;Cono et al, 2019;Hamm et al, 2019).…”

Undinarchaeota illuminate the evolution of DPANN archaea

“…In agreement with our predictions, these analyses yielded phylogenetic trees with various highly supported clusters among unrelated taxa (Supplementary Information). For instance, analyses based on the 25% lowest ranking markers recovered Nanoarchaeota as members of the TACK archaea ( Supplementary Figure 47 ) and Nanohaloarchaeota as a sister lineage of Halobacteria (either as a separate cluster ( Supplementary Figure 46 ) or with DPANN archaea ( Supplementary Figure 47) , in agreement with known symbiont-host relationships 16,17,23 . This is particularly notable because we did not a priori penalize trees in which certain DPANN lineages branch with certain other archaeal lineages ( Supplementary Tables 4-5 ).…”

“…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 .…”

“…The few members that have been successfully enriched in co-culture were shown to represent obligate ectosymbionts dependent on archaeal hosts for growth and survival. 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 .…”