Comparative Genomics Provides Insights into the Genetic Diversity and Evolution of the DPANN Superphylum

Li, Liangzhi; Liu, Zhenghua; Zhou, Zhi; Zhang, Min; Meng, Delong; Liu, Xueduan; Huang, Ye; Li, Xiu-Tong; Jiang, Zhen; Zhong, Shuiping; Drewniak, Łukasz; Yang, Zhi; Li, Qian; Liu, Yongjun; Nan, Xiaolong; Jiang, Biguang; Jiang, Cheng‐Ying; Yin, Huaqun

doi:10.1128/msystems.00602-21

Cited by 12 publications

(12 citation statements)

References 165 publications

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“…In host-associated microbiomes, genetic drift, deletion biases and low populations sizes drive the reduction of genomes ( Li et al, 2021 ). In these environments, the differing levels of intimacy with their host can influence the evolution of the genome of microorganisms.…”

Section: Impact Of Ecosystem and Trophic Strategy On Genome Sizementioning

confidence: 99%

A Genomic Perspective Across Earth’s Microbiomes Reveals That Genome Size in Archaea and Bacteria Is Linked to Ecosystem Type and Trophic Strategy

et al. 2022

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Our view of genome size in Archaea and Bacteria has remained skewed as the data has been dominated by genomes of microorganisms that have been cultivated under laboratory settings. However, the continuous effort to catalog Earth’s microbiomes, specifically propelled by recent extensive work on uncultivated microorganisms, provides an opportunity to revise our perspective on genome size distribution. We present a meta-analysis that includes 26,101 representative genomes from 3 published genomic databases; metagenomic assembled genomes (MAGs) from GEMs and stratfreshDB, and isolates from GTDB. Aquatic and host-associated microbial genomes present on average the smallest estimated genome sizes (3.1 and 3.0 Mbp, respectively). These are followed by terrestrial microbial genomes (average 3.7 Mbp), and genomes from isolated microorganisms (average 4.3 Mbp). On the one hand, aquatic and host-associated ecosystems present smaller genomes sizes in genera of phyla with genome sizes above 3 Mbp. On the other hand, estimated genome size in phyla with genomes under 3 Mbp showed no difference between ecosystems. Moreover, we observed that when using 95% average nucleotide identity (ANI) as an estimator for genetic units, only 3% of MAGs cluster together with genomes from isolated microorganisms. Although there are potential methodological limitations when assembling and binning MAGs, we found that in genome clusters containing both environmental MAGs and isolate genomes, MAGs were estimated only an average 3.7% smaller than isolate genomes. Even when assembly and binning methods introduce biases, estimated genome size of MAGs and isolates are very similar. Finally, to better understand the ecological drivers of genome size, we discuss on the known and the overlooked factors that influence genome size in different ecosystems, phylogenetic groups, and trophic strategies.

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Section: Impact Of Ecosystem and Trophic Strategy On Genome Sizementioning

confidence: 99%

A Genomic Perspective Across Earth’s Microbiomes Reveals That Genome Size in Archaea and Bacteria Is Linked to Ecosystem Type and Trophic Strategy

et al. 2022

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“…Members of DPANN (an acronym of the names of the first included phyla Diapherotrites, Parvarchaeota, Aenigmarchaeota, Nanohaloarchaeota, and Nanoarchaeota), an archaeal superphylum composed of at least 10 of these tentative phyla, inhabit extremely diverse environments (e.g., brackish/freshwater, ocean sediments, hydrothermal vents, acid mine drainage [AMD] sites, hypersaline lakes, permafrost, and the human microbiome) ( 2 ). They share small cell and genome sizes and are generally considered obligate symbionts dependent on other microorganisms ( 3 ), whereas some of them are suggested to possess a free-living lifestyle [i.e., “ Candidatus Altiarchaeota” ( 4 ) and “ Candidatus Diapherotrites” ( 5 )]. However, while many draft/complete genome sequences of DPANN archaea are available, in addition to a considerable number of predictions of biological functions, only a few examples of their successful laboratory cultivation have been reported.…”

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confidence: 99%

Insight into the symbiotic lifestyle of DPANN archaea revealed by cultivation and genome analyses

Sakai

Nur²,

Kato

et al. 2022

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

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Decades of culture-independent analyses have resulted in proposals of many tentative archaeal phyla with no cultivable representative. Members of DPANN (an acronym of the names of the first included phyla Diapherotrites, Parvarchaeota, Aenigmarchaeota, Nanohaloarchaeota, and Nanoarchaeota), an archaeal superphylum composed of at least 10 of these tentative phyla, are generally considered obligate symbionts dependent on other microorganisms. While many draft/complete genome sequences of DPANN archaea are available and their biological functions have been considerably predicted, only a few examples of their successful laboratory cultivation have been reported, limiting our knowledge of their symbiotic lifestyles. Here, we investigated physiology, morphology, and host specificity of an archaeon of the phylum “Candidatus Micrarchaeota” (ARM-1) belonging to the DPANN superphylum by cultivation. We constructed a stable coculture system composed of ARM-1 and its original host Metallosphaera sp. AS-7 belonging to the order Sulfolobales. Further host-switching experiments confirmed that ARM-1 grew on five different archaeal species from three genera—Metallosphaera, Acidianus, and Saccharolobus—originating from geologically distinct hot, acidic environments. The results suggested the existence of DPANN archaea that can grow by relying on a range of hosts. Genomic analyses showed inferred metabolic capabilities, common/unique genetic contents of ARM-1 among cultivated micrarchaeal representatives, and the possibility of horizontal gene transfer between ARM-1 and members of the order Sulfolobales. Our report sheds light on the symbiotic lifestyles of DPANN archaea and will contribute to the elucidation of their biological/ecological functions.

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“…While most ODZ DPANN genomes suggest a host-associated rather than free-living lifestyle, SpSt-1190 genomes average 4 Mb in size, possess a number of biosynthesis pathways, and carry pathways for methanogenesis. These unique archaea may represent free-living DPANN organisms (82)(83)(84) involved in methane cycling. The identification of ODZ DPANN hosts, whether a single host, various hosts, or a community, may hold keys to their distribution and survival within ODZ environments.…”

Section: Discussionmentioning

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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Comparative Genomics Provides Insights into the Genetic Diversity and Evolution of the DPANN Superphylum

Abstract: The domain Archaea is a key research model for gaining insights into the origin and evolution of life, as well as the relevant biogeochemical processes. The discovery of nanosized DPANN archaea has overthrown many aspects of microbiology.

Cited by 12 publications

References 165 publications

A Genomic Perspective Across Earth’s Microbiomes Reveals That Genome Size in Archaea and Bacteria Is Linked to Ecosystem Type and Trophic Strategy

A Genomic Perspective Across Earth’s Microbiomes Reveals That Genome Size in Archaea and Bacteria Is Linked to Ecosystem Type and Trophic Strategy

Insight into the symbiotic lifestyle of DPANN archaea revealed by cultivation and genome analyses

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

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