A new symbiotic nanoarchaeote (Candidatus Nanoclepta minutus) and its host (Zestosphaera tikiterensis gen. nov., sp. nov.) from a New Zealand hot spring

John, Emily St.; Liu, Yitai; Podar, Mircea; Stott, Matthew B.; Meneghin, Jennifer; Chen, Zhiqiang; Lagutin, Kirill; Mitchell, Kevin; Reysenbach, Anna‐Louise

doi:10.1016/j.syapm.2018.08.005

Cited by 88 publications

(58 citation statements)

References 103 publications

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“…On the other hand, these two tightly associated species do not appear to be involved in rampant gene exchange. Unlike acidophilic members of DPANN superphylum, which have several clusters of orthologous genes shared between the ectosymbiont and the host 24,34 , the nanohaloarchaeal genome shows no synteny with the host genome except for the ancestrally collinear loci coding for ribosomal proteins, suggesting no recent transfer of chromosomal fragments between the two (Supplementary Fig. 9).…”

Section: Resultsmentioning

confidence: 99%

“…To date, few finished genome sequences are available for the representatives of DPANN superphylum, and difficulties in their cultivation prevented proper characterization of their growth requirements, morphology and physiology. Only ectosymbiotic and ectoparasitic thermophiles from the candidate phylum Nanoarchaeota and acidophiles from the candidate phylum Micrarchaeota have been obtained in stable binary co-cultures with their hosts from the phyla Crenarchaeota and Euryachaeota, respectively 21-24 . Most recently, the study of enrichment cultures containing members of nanohaloarchaea ( Ca .…”

Section: Introductionmentioning

confidence: 99%

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

Cono

Messina

Rohde

et al. 2019

Preprint

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Nanohaloarchaeota, a clade of diminutive archaea, with small genomes and limited metabolic capabilities, are ubiquitous in hypersaline habitats, which they share with the extremely halophilic and phylogenetically distant euryarchaea. Some of these nanohaloarchaeota and euryarchaea appear to interact with each other. In this study, we investigate the genetic and physiological nature of their relationship. We isolated the nanohaloarchaeon Candidatus Nanohalobium constans LC1Nh and the haloarchaeon Halomicrobium sp. LC1Hm from a solar saltern, reproducibly co-cultivated these species, sequenced their genomes, and characterized their metabolic/trophic interactions. The nanohaloarchaeon is a magnesium-dependent aerotolerant heterotrophic anaerobe of the DPANN superphylum; it lacks respiratory complexes and its energy production relies on fermentative metabolism of sugar derivatives, obtained by depolymerizing alpha-glucans or by acquiring the chitin monomer N-acetylglucosamine from the chitinolytic haloarchaeal host. Halomicrobium is a member of the class Halobacteria and a chitinotrophic aerobe. The nanohaloarchaeon lacks key biosynthetic pathways and is likely to be provided with amino acids, lipids, nucleotides and cofactors via physical contact with its host Halomicrobium. In turn, the ability of Ca. Nanohalobium to hydrolyse alpha-glucans boosts the host’s growth in the absence of a chitin substrate. These findings suggest that at least some members of the nanohaloarchaea, previously considered ecologically unimportant given their limited metabolic potential, in fact may play significant roles in the microbial carbon turnover, food chains, and ecosystem function. The behaviour of Halomicrobium, which accommodates the colonization by Ca. Nanohalobium, can be interpreted as a bet-hedging strategy, maximizing its long-term fitness in a habitat where the availability of carbon substrates can vary both spatially and temporarily.

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Section: Resultsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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

Cono

Messina

Rohde

et al. 2019

Preprint

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“…The dilution-to-extinction approach, followed by filtration and coculture reconstruction, was recently successfully applied for isolation of the nanoarchaeon Ca. Nanoclepta minutus with its host, the thermophilic crenarchaeon Zestosphaera tikiterensis (27). Here, we applied a similar strategy and obtained a binary culture of a nanohaloarchaeon, Ca.…”

Section: Discussionmentioning

confidence: 99%

Symbiosis between nanohaloarchaeon and haloarchaeon is based on utilization of different polysaccharides

Cono

Messina

Rohde

et al. 2020

Proc. Natl. Acad. Sci. U.S.A.

111

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Nano-sized archaeota, with their small genomes and limited metabolic capabilities, are known to associate with other microbes, thereby compensating for their own auxotrophies. These diminutive and yet ubiquitous organisms thrive in hypersaline habitats that they share with haloarchaea. Here, we reveal the genetic and physiological nature of a nanohaloarchaeon–haloarchaeon association, with both microbes obtained from a solar saltern and reproducibly cultivated together in vitro. The nanohaloarchaeon Candidatus Nanohalobium constans LC1Nh is an aerotolerant, sugar-fermenting anaerobe, lacking key anabolic machinery and respiratory complexes. The nanohaloarchaeon cells are found physically connected to the chitinolytic haloarchaeon Halomicrobium sp. LC1Hm. Our experiments revealed that this haloarchaeon can hydrolyze chitin outside the cell (to produce the monosaccharide N-acetylglucosamine), using this beta-glucan to obtain carbon and energy for growth. However, LC1Hm could not metabolize either glycogen or starch (both alpha-glucans) or other polysaccharides tested. Remarkably, the nanohaloarchaeon’s ability to hydrolyze glycogen and starch to glucose enabled growth of Halomicrobium sp. LC1Hm in the absence of a chitin. These findings indicated that the nanohaloarchaeon–haloarchaeon association is both mutualistic and symbiotic; in this case, each microbe relies on its partner’s ability to degrade different polysaccharides. This suggests, in turn, that other nano-sized archaeota may also be beneficial for their hosts. Given that availability of carbon substrates can vary both spatially and temporarily, the susceptibility of Halomicrobium to colonization by Ca. Nanohalobium can be interpreted as a strategy to maximize the long-term fitness of the host.

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“…These include two MAGs related to Acidilobus saccharovorans (each with 81% RpoB amino acid identity), a MAG related to Thermogladius calderae (87% ID), a MAG related to Thermoproteusuzoniensis (97% ID), a MAG related to Caldivirga maquilingensis (94% ID), a MAG related to Pyrobaculum aerophilum (92% ID), a MAG related to Thermofilum carboxydotrophus (100% ID), a MAG related to Vulcanisaeta distributa (93% ID), two MAGs related to Fervidicoccus fontis (71% and 79% ID), a MAG related to Thermocrinis ruber (98% ID) and a Thaumarchaeote‐associated MAG (Supporting Information Appendix S1). Further, a divergent MAG that is distantly related to a S 2 O 3 2− reducing Desulfurococcales strain (e.g., 63% ID to Zestosphaera tikiterensis (St. John et al ., )) was identified that exhibited the metabolic potential for anaerobic S° reduction.…”

Section: Resultsmentioning

confidence: 99%

Geologic legacy spanning >90 years explains unique Yellowstone hot spring geochemistry and biodiversity

Payne

Dunham

Mohr

et al. 2019

Environmental Microbiology

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Summary Little is known about how the geological history of an environment shapes its physical and chemical properties and how these, in turn, influence the assembly of communities. Evening primrose (EP), a moderately acidic hot spring (pH 5.6, 77.4°C) in Yellowstone National Park (YNP), has undergone dramatic physicochemical change linked to seismic activity. Here, we show that this legacy of geologic change led to the development of an unusual sulphur‐rich, anoxic chemical environment that supports a unique archaeal‐dominated and anaerobic microbial community. Metagenomic sequencing and informatics analyses reveal that >96% of this community is supported by dissimilatory reduction or disproportionation of inorganic sulphur compounds, including a novel, deeply diverging sulphate‐reducing thaumarchaeote. When compared to other YNP metagenomes, the inferred functions of EP populations were like those from sulphur‐rich acidic springs, suggesting that sulphur may overprint the predominant influence of pH on the composition of hydrothermal communities. Together, these observations indicate that the dynamic geological history of EP underpins its unique geochemistry and biodiversity, emphasizing the need to consider the legacy of geologic change when describing processes that shape the assembly of communities.

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A new symbiotic nanoarchaeote (Candidatus Nanoclepta minutus) and its host (Zestosphaera tikiterensis gen. nov., sp. nov.) from a New Zealand hot spring

Cited by 88 publications

References 103 publications

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

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

Symbiosis between nanohaloarchaeon and haloarchaeon is based on utilization of different polysaccharides

Geologic legacy spanning >90 years explains unique Yellowstone hot spring geochemistry and biodiversity

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