The parasitic lifestyle of an archaeal symbiont.
Journal
Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555
Informations de publication
Date de publication:
31 Jul 2024
31 Jul 2024
Historique:
received:
26
04
2024
accepted:
25
06
2024
medline:
1
8
2024
pubmed:
1
8
2024
entrez:
31
7
2024
Statut:
epublish
Résumé
DPANN archaea are a diverse group of microorganisms characterised by small cells and reduced genomes. To date, all cultivated DPANN archaea are ectosymbionts that require direct cell contact with an archaeal host species for growth and survival. However, these interactions and their impact on the host species are poorly understood. Here, we show that a DPANN archaeon (Candidatus Nanohaloarchaeum antarcticus) engages in parasitic interactions with its host (Halorubrum lacusprofundi) that result in host cell lysis. During these interactions, the nanohaloarchaeon appears to enter, or be engulfed by, the host cell. Our results provide experimental evidence for a predatory-like lifestyle of an archaeon, suggesting that at least some DPANN archaea may have roles in controlling host populations and their ecology.
Identifiants
pubmed: 39085207
doi: 10.1038/s41467-024-49962-y
pii: 10.1038/s41467-024-49962-y
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
6449Informations de copyright
© 2024. The Author(s).
Références
Hamm, J. N. et al. Unexpected host dependency of Antarctic Nanohaloarchaeota. Proc. Natl Acad. Sci. USA 116, 14661–14670 (2019).
pubmed: 31253704
pmcid: 6642349
doi: 10.1073/pnas.1905179116
Huber, H. et al. A new phylum of Archaea represented by a nanosized hyperthermophilic symbiont. Nature 417, 63–67 (2002).
pubmed: 11986665
doi: 10.1038/417063a
Liu, X. et al. Insights into the ecology, evolution, and metabolism of the widespread Woesearchaeotal lineages. Microbiome 6, 102 (2018).
pubmed: 29884244
pmcid: 5994134
doi: 10.1186/s40168-018-0488-2
Baker, B. J. et al. Enigmatic, ultrasmall, uncultivated Archaea. Proc. Natl Acad. Sci. USA 107, 8806–8811 (2010).
pubmed: 20421484
pmcid: 2889320
doi: 10.1073/pnas.0914470107
Narasingarao, P. et al. De novo metagenomic assembly reveals abundant novel major lineage of Archaea in hypersaline microbial communities. ISME J. 6, 81–93 (2012).
pubmed: 21716304
doi: 10.1038/ismej.2011.78
Koskinen, K. et al. First insights into the diverse human archaeome: specific detection of archaea in the gastrointestinal tract, lung, and nose and on skin. Mbio 8, 6 (2017).
doi: 10.1128/mBio.00824-17
Castelle, C. J. & Banfield, J. F. Major new microbial groups expand diversity and alter our understanding of the tree of life. Cell 172, 1181–1197 (2018).
pubmed: 29522741
doi: 10.1016/j.cell.2018.02.016
Dombrowski, N. et al. Undinarchaeota illuminate DPANN phylogeny and the impact of gene transfer on archaeal evolution. Nat. Commun. 11, 3939 (2020).
pubmed: 32770105
pmcid: 7414124
doi: 10.1038/s41467-020-17408-w
Dombrowski, N., Lee, J. H., Williams, T. A., Offre, P. & Spang, A. Genomic diversity, lifestyles and evolutionary origins of DPANN archaea. FEMS Microbiol. Lett. 366, 2 (2019).
doi: 10.1093/femsle/fnz008
Tully, B. J., Graham, E. D. & Heidelberg, J. F. The reconstruction of 2,631 draft metagenome-assembled genomes from the global oceans. Sci. Data 5, 170203 (2018).
pubmed: 29337314
pmcid: 5769542
doi: 10.1038/sdata.2017.203
Vavourakis, C. D. et al. Metagenomic insights into the uncultured diversity and physiology of microbes in four hypersaline soda lake brines. Front. Microbiol. 7, 211 (2016).
pubmed: 26941731
pmcid: 4766312
doi: 10.3389/fmicb.2016.00211
Xie, Y. G. et al. Functional differentiation determines the molecular basis of the symbiotic lifestyle of Ca. nanohaloarchaeota. Microbiome 10, 172 (2022).
pubmed: 36242054
pmcid: 9563170
doi: 10.1186/s40168-022-01376-y
St John, E. et al. A new symbiotic nanoarchaeote (Candidatus Nanoclepta minutus) and its host (Zestosphaera tikiterensis gen. nov., sp. nov.) from a New Zealand hot spring. Syst. Appl. Microbiol. 42, 94–106 (2019).
doi: 10.1016/j.syapm.2018.08.005
Wurch, L. et al. Genomics-informed isolation and characterization of a symbiotic Nanoarchaeota system from a terrestrial geothermal environment. Nat. Commun. 7, 12115 (2016).
pubmed: 27378076
pmcid: 4935971
doi: 10.1038/ncomms12115
Golyshina, O. V. et al. ARMAN’ archaea depend on association with euryarchaeal host in culture and in situ. Nat. Commun. 8, 60 (2017).
pubmed: 28680072
pmcid: 5498576
doi: 10.1038/s41467-017-00104-7
Krause, S. et al. The importance of biofilm formation for cultivation of a Micrarchaeon and its interactions with its Thermoplasmatales host. Nat. Commun. 13, 1735 (2022).
pubmed: 35365607
pmcid: 8975820
doi: 10.1038/s41467-022-29263-y
La Cono, V. et al. Symbiosis between nanohaloarchaeon and haloarchaeon is based on utilization of different polysaccharides. Proc. Natl Acad. Sci. USA 117, 20223–20234 (2020).
pubmed: 32759215
pmcid: 7443923
doi: 10.1073/pnas.2007232117
Reva O., et al. Functional diversity of nanohaloarchaea within xylan-degrading consortia. Front. Microbiol. 14 1182464 (2023).
Heimerl, T. et al. A complex endomembrane system in the Archaeon Ignicoccus hospitalis tapped by Nanoarchaeum equitans. Front. Microbiol. 8, 1072 (2017).
pubmed: 28659892
pmcid: 5468417
doi: 10.3389/fmicb.2017.01072
Comolli, L. R. & Banfield, J. F. Inter-species interconnections in acid mine drainage microbial communities. Front. Microbiol. 5, 367 (2014).
pubmed: 25120533
pmcid: 4110969
Liao, Y. et al. Developing a genetic manipulation system for the Antarctic archaeon, Halorubrum lacusprofundi: investigating acetamidase gene function. Sci. Rep. 6, 34639 (2016).
pubmed: 27708407
pmcid: 5052560
doi: 10.1038/srep34639
Gebhard, L. J., Duggin, I. G. & Erdmann, S. Improving the genetic system for Halorubrum lacusprofundi to allow in-frame deletions. Front. Microbiol. 14, 1095621 (2023).
pubmed: 37065119
pmcid: 10102395
doi: 10.3389/fmicb.2023.1095621
Maslov, I. et al. Efficient non-cytotoxic fluorescent staining of halophiles. Sci. Rep. 8, 2549 (2018).
pubmed: 29416075
pmcid: 5803262
doi: 10.1038/s41598-018-20839-7
Tschitschko, B. et al. Genomic variation and biogeography of Antarctic haloarchaea. Microbiome 6, 113 (2018).
pubmed: 29925429
pmcid: 6011602
doi: 10.1186/s40168-018-0495-3
Franzmann, P. D. et al. Halobacterium lacusprofundi sp. nov., a halophilic bacterium isolated from Deep Lake, Antarctica. Syst. Appl. Microbiol. 11, 20–27 (1988).
doi: 10.1016/S0723-2020(88)80044-4
Liao, Y. et al. Morphological and proteomic analysis of biofilms from the Antarctic archaeon, Halorubrum lacusprofundi. Sci. Rep. 6, 37454 (2016).
pubmed: 27874045
pmcid: 5118699
doi: 10.1038/srep37454
von Kügelgen, A., Alva, V. & Bharat, T. A. M. Complete atomic structure of a native archaeal cell surface. Cell Rep. 37, 110052 (2021).
doi: 10.1016/j.celrep.2021.110052
Bharat, T. A. M., von Kügelgen, A. & Alva, V. Molecular logic of prokaryotic surface layer structures. Trends Microbiol. 29, 405–415 (2021).
pubmed: 33121898
pmcid: 8559796
doi: 10.1016/j.tim.2020.09.009
Herdman, M. et al. High-resolution mapping of metal ions reveals principles of surface layer assembly in Caulobacter crescentus cells. Structure 30, 215–228 e215 (2022).
pubmed: 34800371
pmcid: 8828063
doi: 10.1016/j.str.2021.10.012
von Kügelgen, A. et al. In situ structure of an intact lipopolysaccharide-bound bacterial surface layer. Cell 180, 348–358 e315 (2020).
doi: 10.1016/j.cell.2019.12.006
Williams, T. J. et al. Cold adaptation of the Antarctic haloarchaea Halohasta litchfieldiae and Halorubrum lacusprofundi. Environ. Microbiol. 19, 2210–2227 (2017).
pubmed: 28217912
doi: 10.1111/1462-2920.13705
Murphy, D. J. The dynamic roles of intracellular lipid droplets: from archaea to mammals. Protoplasma 249, 541–585 (2012).
pubmed: 22002710
doi: 10.1007/s00709-011-0329-7
Chanyi, R. M. & Koval, S. F. Role of type IV pili in predation by Bdellovibrio bacteriovorus. PLoS One 9, e113404 (2014).
pubmed: 25409535
pmcid: 4237445
doi: 10.1371/journal.pone.0113404
Moreira, D., Zivanovic, Y., Lopez-Archilla, A. I., Iniesto, M. & Lopez-Garcia, P. Reductive evolution and unique predatory mode in the CPR bacterium Vampirococcus lugosii. Nat. Commun. 12, 2454 (2021).
pubmed: 33911080
pmcid: 8080830
doi: 10.1038/s41467-021-22762-4
Xie, B. et al. Type IV pili trigger episymbiotic association of Saccharibacteria with its bacterial host. Proc. Natl Acad. Sci. USA 119, e2215990119 (2022).
pubmed: 36454763
pmcid: 9894109
doi: 10.1073/pnas.2215990119
Kapteijn, R. et al. Endocytosis-like DNA uptake by cell wall-deficient bacteria. Nat. Commun. 13, 5524 (2022).
pubmed: 36138004
pmcid: 9500057
doi: 10.1038/s41467-022-33054-w
Kellner, S. et al. Genome size evolution in the Archaea. Emerg. Top. Life Sci. 2, 595–605 (2018).
pubmed: 33525826
pmcid: 7289037
doi: 10.1042/ETLS20180021
Lind, A. E. et al. Genomes of two archaeal endosymbionts show convergent adaptations to an intracellular lifestyle. ISME J. 12, 2655–2667 (2018).
pubmed: 29991760
pmcid: 6194110
doi: 10.1038/s41396-018-0207-9
Seymour, C. O. et al. Hyperactive nanobacteria with host-dependent traits pervade Omnitrophota. Nat. Microbiol 8, 727–744 (2023).
pubmed: 36928026
pmcid: 10066038
doi: 10.1038/s41564-022-01319-1
Cavicchioli, R. Microbial ecology of Antarctic aquatic systems. Nat. Rev. Microbiol. 13, 691–706 (2015).
pubmed: 26456925
doi: 10.1038/nrmicro3549
Reysenbach, A. L. et al. Complex subsurface hydrothermal fluid mixing at a submarine arc volcano supports distinct and highly diverse microbial communities. Proc. Natl Acad. Sci. USA 117, 32627–32638 (2020).
pubmed: 33277434
pmcid: 7768687
doi: 10.1073/pnas.2019021117
Erdmann, S., Tschitschko, B., Zhong, L., Raftery, M. J. & Cavicchioli, R. A plasmid from an Antarctic haloarchaeon uses specialized membrane vesicles to disseminate and infect plasmid-free cells. Nat. Microbiol. 2, 1446–1455 (2017).
pubmed: 28827601
doi: 10.1038/s41564-017-0009-2
Duggin, I. G. et al. CetZ tubulin-like proteins control archaeal cell shape. Nature 519, 362–365 (2015).
pubmed: 25533961
doi: 10.1038/nature13983
Dyall-Smith M. The Halohandbook: Protocols for Halobacterial Genetics, Version 7.3 https://haloarchaea.com/wp-content/uploads/2018/10/Halohandbook_2009_v7.3mds.pdf (2015).
Schindelin, J. et al. Fiji: an open-source platform for biological-image analysis. Nat. Methods 9, 676–682 (2012).
pubmed: 22743772
doi: 10.1038/nmeth.2019
Ducret, A., Quardokus, E. M. & Brun, Y. V. MicrobeJ, a tool for high throughput bacterial cell detection and quantitative analysis. Nat. Microbiol. 1, 16077 (2016).
pubmed: 27572972
pmcid: 5010025
doi: 10.1038/nmicrobiol.2016.77
Pernthaler J., Glöckner F.-O., Schönhuber W., Amann R. Fluorescence in situ hybridization (FISH) with rRNA-targeted oligonucleotide probes. Methods in Microbiology. (Academic Press, 2001).
Dubochet J., McDowall A. W. Vitrification of pure water for electron microscopy. J. Microsc. 124 RP3–RP4 (1981).
Sulkowski, N. I., Hardy, G. G., Brun, Y. V. & Bharat, T. A. M. A multiprotein complex anchors adhesive holdfast at the outer membrane of Caulobacter crescentus. J. Bacteriol. 201, e00112–e00119 (2019).
pubmed: 31061167
pmcid: 6707917
doi: 10.1128/JB.00112-19
Bharat, T. A. M. & Kukulski, W. CrYo-correlative light and electron microscopy. Correlative Imaging 9, 1369 (2019).
Hoffmann, P. C. et al. Tricalbins contribute to cellular lipid flux and form curved ER-PM contacts that are bridged by rod-shaped structures. Dev. Cell 51, 488–502.e488 (2019).
pubmed: 31743663
pmcid: 6863393
doi: 10.1016/j.devcel.2019.09.019
Hagen, W. J. H., Wan, W. & Briggs, J. A. G. Implementation of a cryo-electron tomography tilt-scheme optimized for high resolution subtomogram averaging. J. Struct. Biol. 197, 191–198 (2017).
pubmed: 27313000
pmcid: 5287356
doi: 10.1016/j.jsb.2016.06.007
Mastronarde, D. N. Automated electron microscope tomography using robust prediction of specimen movements. J. Struct. Biol. 152, 36–51 (2005).
pubmed: 16182563
doi: 10.1016/j.jsb.2005.07.007
Mastronarde, D. N. & Held, S. R. Automated tilt series alignment and tomographic reconstruction in IMOD. J. Struct. Biol. 197, 102–113 (2017).
pubmed: 27444392
doi: 10.1016/j.jsb.2016.07.011
Agulleiro, J. I. & Fernandez, J. J. Tomo3D 2.0–exploitation of advanced vector extensions (AVX) for 3D reconstruction. J. Struct. Biol. 189, 147–152 (2015).
pubmed: 25528570
doi: 10.1016/j.jsb.2014.11.009
Buchholz T. O., Jordan M., Pigino G., Jug F. Cryo-CARE: content-aware image restoration for cryo-transmission electron microscopy data. In Proc. IEEE 16th International Symposium on Biomedical Imaging (ISBI 2019) (2019).
Buchholz, T. O. et al. Content-aware image restoration for electron microscopy. Methods Cell Biol. 152, 277–289 (2019).
pubmed: 31326025
doi: 10.1016/bs.mcb.2019.05.001
Emms, D. M. & Kelly, S. OrthoFinder: solving fundamental biases in whole genome comparisons dramatically improves orthogroup inference accuracy. Genome Biol. 16, 157 (2015).
pubmed: 26243257
pmcid: 4531804
doi: 10.1186/s13059-015-0721-2
Jones, P. et al. InterProScan 5: genome-scale protein function classification. Bioinformatics 30, 1236–1240 (2014).
pubmed: 24451626
pmcid: 3998142
doi: 10.1093/bioinformatics/btu031
Katoh, K. & Standley, D. M. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol. Biol. Evol. 30, 772–780 (2013).
pubmed: 23329690
pmcid: 3603318
doi: 10.1093/molbev/mst010
Criscuolo, A. & Gribaldo, S. BMGE (Block Mapping and Gathering with Entropy): a new software for selection of phylogenetic informative regions from multiple sequence alignments. BMC Evol. Biol. 10, 210 (2010).
pubmed: 20626897
pmcid: 3017758
doi: 10.1186/1471-2148-10-210
Steinegger, M. et al. HH-suite3 for fast remote homology detection and deep protein annotation. BMC Bioinforma. 20, 473 (2019).
doi: 10.1186/s12859-019-3019-7
Quinlan, A. R. & Hall, I. M. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 26, 841–842 (2010).
pubmed: 20110278
pmcid: 2832824
doi: 10.1093/bioinformatics/btq033
Kelley, L. A., Mezulis, S., Yates, C. M., Wass, M. N. & Sternberg, M. J. The Phyre2 web portal for protein modeling, prediction and analysis. Nat. Protoc. 10, 845–858 (2015).
pubmed: 25950237
pmcid: 5298202
doi: 10.1038/nprot.2015.053
Drozdetskiy, A., Cole, C., Procter, J. & Barton, G. J. JPred4: a protein secondary structure prediction server. Nucleic Acids Res. 43, W389–W394 (2015).
pubmed: 25883141
pmcid: 4489285
doi: 10.1093/nar/gkv332
Wu R., et al. High-resolution de novo structure prediction from primary sequence. bioRxiv, 2022.2007.2021.500999 (2022).
van Kempen, M. et al. Fast and accurate protein structure search with Foldseek. Nat. Biotechnol. 42, 243–246 (2023).
pubmed: 37156916
pmcid: 10869269
doi: 10.1038/s41587-023-01773-0
Seemann, T. Prokka: rapid prokaryotic genome annotation. Bioinformatics 30, 2068–2069 (2014).
pubmed: 24642063
doi: 10.1093/bioinformatics/btu153
Makarova, K. S., Wolf, Y. I. & Koonin, E. V. Archaeal clusters of orthologous genes (arCOGs): an update and application for analysis of shared features between thermococcales, methanococcales, and methanobacteriales. Life 5, 818–840 (2015).
pubmed: 25764277
pmcid: 4390880
doi: 10.3390/life5010818
Aramaki, T. et al. KofamKOALA: KEGG ortholog assignment based on profile HMM and adaptive score threshold. Bioinformatics 36, 2251–2252 (2020).
pubmed: 31742321
doi: 10.1093/bioinformatics/btz859
Bateman, A. et al. The Pfam protein families database. Nucleic Acids Res. 32, D138–D141 (2004).
pubmed: 14681378
pmcid: 308855
doi: 10.1093/nar/gkh121
Haft, D. H., Selengut, J. D. & White, O. The TIGRFAMs database of protein families. Nucleic Acids Res. 31, 371–373 (2003).
pubmed: 12520025
pmcid: 165575
doi: 10.1093/nar/gkg128
Yin, Y. et al. dbCAN: a web resource for automated carbohydrate-active enzyme annotation. Nucleic Acids Res. 40, W445–W451 (2012).
pubmed: 22645317
pmcid: 3394287
doi: 10.1093/nar/gks479
Rawlings, N. D. Peptidase specificity from the substrate cleavage collection in the MEROPS database and a tool to measure cleavage site conservation. Biochimie 122, 5–30 (2016).
pubmed: 26455268
pmcid: 4756867
doi: 10.1016/j.biochi.2015.10.003
Saier, M. H. Jr., Tran, C. V. & Barabote, R. D. TCDB: the Transporter Classification Database for membrane transport protein analyses and information. Nucleic Acids Res. 34, D181–D186 (2006).
pubmed: 16381841
doi: 10.1093/nar/gkj001
Sondergaard, D., Pedersen, C. N. & Greening, C. HydDB: a web tool for hydrogenase classification and analysis. Sci. Rep. 6, 34212 (2016).
pubmed: 27670643
pmcid: 5037454
doi: 10.1038/srep34212
Altschul, S. F. et al. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25, 3389–3402 (1997).
pubmed: 9254694
pmcid: 146917
doi: 10.1093/nar/25.17.3389
Finn, R. D., Clements, J. & Eddy, S. R. HMMER web server: interactive sequence similarity searching. Nucleic Acids Res. 39, W29–W37 (2011).
pubmed: 21593126
pmcid: 3125773
doi: 10.1093/nar/gkr367
Chaumeil, P. A., Mussig, A. J., Hugenholtz, P. & Parks, D. H. GTDB-Tk: a toolkit to classify genomes with the Genome Taxonomy Database. Bioinformatics 36, 1925–1927 (2019).
pubmed: 31730192
pmcid: 7703759
doi: 10.1093/bioinformatics/btz848
Darling, A. E. et al. PhyloSift: phylogenetic analysis of genomes and metagenomes. PeerJ 2, e243 (2014).
pubmed: 24482762
pmcid: 3897386
doi: 10.7717/peerj.243
Nguyen, L. T., Schmidt, H. A., von Haeseler, A. & Minh, B. Q. IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol. Biol. Evol. 32, 268–274 (2015).
pubmed: 25371430
doi: 10.1093/molbev/msu300