Ultra-small bacteria and archaea exhibit genetic flexibility towards groundwater oxygen content, and adaptations for attached or planktonic lifestyles

Gios, Emilie; Mosley, Olivia E.; Weaver, Louise; Close, Murray E.; Daughney, Christopher J.

doi:10.1038/s43705-023-00223-x

Cited by 10 publications

(7 citation statements)

References 98 publications

(172 reference statements)

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“…Two unique DPANN MAGs (Arabian11_MAG21 and ETNP3_MAG14) also carried the A and B subunits of assimilatory anaerobic sulfite reductase, but none carried dissimilatory sulfur cycling genes. Additionally, several DPANN MAGs contained desulfoferredoxin, manganese superoxide dismutases, and thioredoxin, which are involved in antioxidant systems ( 16 ), despite living in anoxic water columns. Formaldehyde assimilation genes were found within a number of Woesearchaeota MAGs, suggesting the ability to use one-carbon compounds for growth.…”

Section: Resultsmentioning

confidence: 99%

“…Since their discovery, DPANN archaea have been found in a variety of diverse environments, including hydrothermal vents ( 12 ), freshwater and hypersaline lakes ( 13 , 14 ), groundwater ( 15 , 16 ), terrestrial hot springs ( 17 ), marine sediments and water columns ( 12 , 18 , 19 ), and the Black Sea ( 20 ). Archaea writ large play crucial roles in global biogeochemical cycles, such as in ammonia oxidation ( 21 ), methane cycling ( 22 ), and organic carbon scavenging ( 23 ), and DPANN archaea have been found to possess genes for sulfur cycling and organic substrate degradation ( 15 , 18 ).…”

Section: Introductionmentioning

confidence: 99%

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Uncultivated DPANN archaea are ubiquitous inhabitants of global oxygen-deficient zones with diverse metabolic potential

Zhang,

Borer,

Zhao

et al. 2024

mBio

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Archaea belonging to the DPANN (Diapherotrites, Parvarchaeota, Aenigmarchaeota, Nanoarchaeota, and Nanohaloarchaeota) superphylum have been found in an expanding number of environments and perform a variety of biogeochemical roles, including contributing to carbon, sulfur, and nitrogen cycling. Generally characterized by ultrasmall cell sizes and reduced genomes, DPANN archaea may form mutualistic, commensal, or parasitic interactions with various archaeal and bacterial hosts, influencing the ecology and functioning of microbial communities. While DPANN archaea reportedly comprise a sizeable fraction of the archaeal community within marine oxygen-deficient zone (ODZ) water columns, little is known about their metabolic capabilities in these ecosystems. We report 33 novel metagenome-assembled genomes (MAGs) belonging to the DPANN phyla Nanoarchaeota, Pacearchaeota, Woesearchaeota, Undinarchaeota, Iainarchaeota, and SpSt-1190 from pelagic ODZs in the Eastern Tropical North Pacific and the Arabian Sea. We find these archaea to be permanent, stable residents of all three major ODZs only within anoxic depths, comprising up to 1% of the total microbial community and up to 25%–50% of archaea as estimated from read mapping to MAGs. ODZ DPANN appear to be capable of diverse metabolic functions, including fermentation, organic carbon scavenging, and the cycling of sulfur, hydrogen, and methane. Within a majority of ODZ DPANN, we identify a gene homologous to nitrous oxide reductase. Modeling analyses indicate the feasibility of a nitrous oxide reduction metabolism for host-attached symbionts, and the small genome sizes and reduced metabolic capabilities of most DPANN MAGs suggest host-associated lifestyles within ODZs. IMPORTANCE Archaea from the DPANN (Diapherotrites, Parvarchaeota, Aenigmarchaeota, Nanoarchaeota, and Nanohaloarchaeota) superphylum have diverse metabolic capabilities and participate in multiple biogeochemical cycles. While metagenomics and enrichments have revealed that many DPANN are characterized by ultrasmall genomes, few biosynthetic genes, and episymbiotic lifestyles, much remains unknown about their biology. We report 33 new DPANN metagenome-assembled genomes originating from the three global marine oxygen-deficient zones (ODZs), the first from these regions. We survey DPANN abundance and distribution within the ODZ water column, investigate their biosynthetic capabilities, and report potential roles in the cycling of organic carbon, methane, and nitrogen. We test the hypothesis that nitrous oxide reductases found within several ODZ DPANN genomes may enable ultrasmall episymbionts to serve as nitrous oxide consumers when attached to a host nitrous oxide producer. Our results indicate DPANN archaea as ubiquitous residents within the anoxic core of ODZs with the potential to produce or consume key compounds.

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Section: Resultsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Uncultivated DPANN archaea are ubiquitous inhabitants of global oxygen-deficient zones with diverse metabolic potential

Zhang,

Borer,

Zhao

et al. 2024

mBio

View full text Add to dashboard Cite

show abstract

“…Two DPANN MAGs also carried the A and B subunits of assimilatory anaerobic sulfite reductase, but none carried dissimilatory sulfur cycling genes. Additionally, several DPANN MAGs contain desulfoferredoxin, manganese superoxide dismutases, and thioredoxin, which are involved in antioxidant systems (14), despite living in anoxic water columns. Formaldehyde assimilation genes were found within a number of Woesarchaeota MAGs, suggesting the ability to use one-carbon compounds for growth.…”

Section: Resultsmentioning

confidence: 99%

“…Since their discovery, DPANN archaea have been found in a variety of diverse environments, including hydrothermal vents (10), freshwater and hypersaline lakes (11, 12), groundwater (13, 14), terrestrial hot springs (15), marine sediments and water columns (10, 16, 17), and the Black Sea (18). Archaea writ large play crucial roles in global biogeochemical cycles, such as in ammonia oxidation (19), methane cycling (20), and organic carbon scavenging (21), and DPANN archaea have been found to possess genes for sulfur cycling and organic substrate degradation (13, 16).…”

Section: Introductionmentioning

confidence: 99%

Uncultivated DPANN archaea are ubiquitous inhabitants of global oxygen deficient zones with diverse metabolic potential

Zhang,

Borer,

Zhao

et al. 2023

Preprint

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Archaea belonging to the DPANN superphylum have been found within an expanding number of environments and perform a variety of biogeochemical roles, including contributing to carbon, sulfur, and nitrogen cycling. Generally characterized by ultrasmall cell sizes and reduced genomes, DPANN archaea may form mutualistic, commensal, or parasitic interactions with various archaeal and bacterial hosts, influencing the ecology and functioning of microbial communities. While DPANN archaea reportedly comprise 15–26% of the archaeal community within marine oxygen deficient zone (ODZ) water columns, little is known about their metabolic capabilities in these ecosystems. We report 33 novel metagenome-assembled genomes belonging to DPANN phyla Nanoarchaeota, Pacearchaeota, Woesarchaeota, Undinarchaeota, Iainarchaeota, and SpSt-1190 from pelagic ODZs in the Eastern Tropical North Pacific and Arabian Sea. We find these archaea to be permanent, stable residents of all 3 major ODZs only within anoxic depths, comprising up to 1% of the total microbial community and up to 25–50% of archaea. ODZ DPANN appear capable of diverse metabolic functions, including fermentation, organic carbon scavenging, and the cycling of sulfur, hydrogen, and methane. Within a majority of ODZ DPANN, we identify a gene homologous to nitrous oxide reductase. Modeling analyses indicate the feasibility of a nitrous oxide reduction metabolism for host-attached symbionts, and the small genome sizes and reduced metabolic capabilities of most DPANN MAGs suggest host-associated lifestyles within ODZs.ImportanceArchaea from the DPANN superphylum have diverse metabolic capabilities and participate in multiple biogeochemical cycles. While metagenomics and enrichments have revealed that many DPANN are characterized by ultrasmall genomes, few biosynthetic genes, and episymbiotic lifestyles, much remains unknown about their biology. We report 33 new DPANN metagenome-assembled genomes originating from the 3 global marine oxygen deficient zones (ODZs), the first from these regions. We survey DPANN abundance and distribution within the ODZ water column, investigate their biosynthetic capabilities, and report potential roles in the cycling of organic carbon, methane, and nitrogen. We test the hypothesis that nitrous oxide reductases found within several ODZ DPANN genomes may enable ultrasmall episymbionts to serve as nitrous oxide consumers when attached to a host nitrous oxide producer. Our results indicate DPANN archaea as ubiquitous residents within the anoxic core of ODZs with the potential to produce or consume key compounds.

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“…CPRs include more than 70 phyla, with around 11,000 genomes, most of which are incomplete and considered as metagenome-assembled genomes (MAGs) in the National Center for Biotechnology Information (NCBI) database [ 26 ]. CPRs are also sometimes referred to as “Patescibacteria”, since more than 74% of their genomes belong to this superphylum or phylum [ 27 , 28 ]. Nevertheless, the distinction between superphylum and phylum has not yet been clearly described for this radiation.…”

Section: Introduction: Progress In High-throughput Technologies Enabl...mentioning

confidence: 99%

Using Genomics to Decipher the Enigmatic Properties and Survival Adaptation of Candidate Phyla Radiation

2023

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Microbial ecology is a critical field for understanding the composition, diversity, and functions of microorganisms in various environmental and health-related processes. The discovery of Candidate Phyla Radiation (CPR) through culture-independent methods has introduced a new division of microbes characterized by a symbiotic/parasitic lifestyle, small cell size, and small genome. Despite being poorly understood, CPRs have garnered significant attention in recent years due to their widespread detection in a variety of environmental and clinical samples. These microorganisms have been found to exhibit a high degree of genetic diversity compared to other microbes. Several studies have shed light on their potential importance in global biogeochemical cycles and their impact on various human activities. In this review, we provide a systematic overview of the discovery of CPRs. We then focus on describing how the genomic characteristics of CPRs have helped them interact with and adapt to other microbes in different ecological niches. Future works should focus on discovering the metabolic capacities of CPRs and, if possible, isolating them to obtain a better understanding of these microorganisms.

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Ultra-small bacteria and archaea exhibit genetic flexibility towards groundwater oxygen content, and adaptations for attached or planktonic lifestyles

Cited by 10 publications

References 98 publications

Uncultivated DPANN archaea are ubiquitous inhabitants of global oxygen-deficient zones with diverse metabolic potential

Uncultivated DPANN archaea are ubiquitous inhabitants of global oxygen-deficient zones with diverse metabolic potential

Uncultivated DPANN archaea are ubiquitous inhabitants of global oxygen deficient zones with diverse metabolic potential

Using Genomics to Decipher the Enigmatic Properties and Survival Adaptation of Candidate Phyla Radiation

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