Comparative Genomics Provides Insights into the Genetic Diversity and Evolution of the DPANN Superphylum
ABSTRACT DPANN is known as highly diverse, globally widespread, and mostly ectosymbiotic archaeal superphylum. However, this group of archaea was overlooked for a long time, and there were limited in-depth studies reported. In this investigation, 41 metagenome-assembled genomes (MAGs) belonging to t...
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American Society for Microbiology
2021-08-01
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Series: | mSystems |
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Online Access: | https://journals.asm.org/doi/10.1128/mSystems.00602-21 |
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doaj-fb3f4cef6db042a38f19cb68c4e6c175 |
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record_format |
Article |
collection |
DOAJ |
language |
English |
format |
Article |
sources |
DOAJ |
author |
Liangzhi Li Zhenghua Liu Zhicheng Zhou Min Zhang Delong Meng Xueduan Liu Ye Huang Xiutong Li Zhen Jiang Shuiping Zhong Lukasz Drewniak Zhendong Yang Qian Li Yongjun Liu Xiaolong Nan Biguang Jiang Chengying Jiang Huaqun Yin |
spellingShingle |
Liangzhi Li Zhenghua Liu Zhicheng Zhou Min Zhang Delong Meng Xueduan Liu Ye Huang Xiutong Li Zhen Jiang Shuiping Zhong Lukasz Drewniak Zhendong Yang Qian Li Yongjun Liu Xiaolong Nan Biguang Jiang Chengying Jiang Huaqun Yin Comparative Genomics Provides Insights into the Genetic Diversity and Evolution of the DPANN Superphylum mSystems DPANN superphylum evolution genome reduction lateral gene transfer comparative genomics |
author_facet |
Liangzhi Li Zhenghua Liu Zhicheng Zhou Min Zhang Delong Meng Xueduan Liu Ye Huang Xiutong Li Zhen Jiang Shuiping Zhong Lukasz Drewniak Zhendong Yang Qian Li Yongjun Liu Xiaolong Nan Biguang Jiang Chengying Jiang Huaqun Yin |
author_sort |
Liangzhi Li |
title |
Comparative Genomics Provides Insights into the Genetic Diversity and Evolution of the DPANN Superphylum |
title_short |
Comparative Genomics Provides Insights into the Genetic Diversity and Evolution of the DPANN Superphylum |
title_full |
Comparative Genomics Provides Insights into the Genetic Diversity and Evolution of the DPANN Superphylum |
title_fullStr |
Comparative Genomics Provides Insights into the Genetic Diversity and Evolution of the DPANN Superphylum |
title_full_unstemmed |
Comparative Genomics Provides Insights into the Genetic Diversity and Evolution of the DPANN Superphylum |
title_sort |
comparative genomics provides insights into the genetic diversity and evolution of the dpann superphylum |
publisher |
American Society for Microbiology |
series |
mSystems |
issn |
2379-5077 |
publishDate |
2021-08-01 |
description |
ABSTRACT DPANN is known as highly diverse, globally widespread, and mostly ectosymbiotic archaeal superphylum. However, this group of archaea was overlooked for a long time, and there were limited in-depth studies reported. In this investigation, 41 metagenome-assembled genomes (MAGs) belonging to the DPANN superphylum were recovered (18 MAGs had average nucleotide identity [ANI] values of <95% and a percentage of conserved proteins [POCP] of >50%, while 14 MAGs showed a POCP of <50%), which were analyzed comparatively with 515 other published DPANN genomes. Mismatches to known 16S rRNA gene primers were identified among 16S rRNA genes of DPANN archaea. Numbers of gene families lost (mostly related to energy and amino acid metabolism) were over three times greater than those gained in the evolution of DPANN archaea. Lateral gene transfer (LGT; ∼45.5% was cross-domain) had facilitated niche adaption of the DPANN archaea, ensuring a delicate equilibrium of streamlined genomes with efficient niche-adaptive strategies. For instance, LGT-derived cytochrome bd ubiquinol oxidase and arginine deiminase in the genomes of “Candidatus Micrarchaeota” could help them better adapt to aerobic acidic mine drainage habitats. In addition, most DPANN archaea acquired enzymes for biosynthesis of extracellular polymeric substances (EPS) and transketolase/transaldolase for the pentose phosphate pathway from Bacteria. IMPORTANCE 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. However, the DPANN superphylum still contains a vast genetic novelty and diversity that need to be explored. Comprehensively comparative genomic analysis on the DPANN superphylum was performed in this study, with an attempt to illuminate its metabolic potential, ecological distribution and evolutionary history. Many interphylum differences within the DPANN superphylum were found. For example, Altiarchaeota had the biggest genome among DPANN phyla, possessing many pathways missing in other phyla, such as formaldehyde assimilation and the Wood-Ljungdahl pathway. In addition, LGT acted as an important force to provide DPANN archaeal genetic flexibility that permitted the occupation of diverse niches. This study has advanced our understanding of the diversity and genome evolution of archaea. |
topic |
DPANN superphylum evolution genome reduction lateral gene transfer comparative genomics |
url |
https://journals.asm.org/doi/10.1128/mSystems.00602-21 |
work_keys_str_mv |
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doaj-fb3f4cef6db042a38f19cb68c4e6c1752021-08-31T13:57:55ZengAmerican Society for MicrobiologymSystems2379-50772021-08-016410.1128/mSystems.00602-21Comparative Genomics Provides Insights into the Genetic Diversity and Evolution of the DPANN SuperphylumLiangzhi Li0Zhenghua Liu1Zhicheng Zhou2Min Zhang3Delong Meng4Xueduan Liu5Ye Huang6Xiutong Li7Zhen Jiang8Shuiping Zhong9Lukasz Drewniak10Zhendong Yang11Qian Li12Yongjun Liu13Xiaolong Nan14Biguang Jiang15Chengying Jiang16Huaqun Yin17School of Minerals Processing and Bioengineering, Central South University, Changsha, ChinaSchool of Minerals Processing and Bioengineering, Central South University, Changsha, ChinaHunan Tobacco Science Institute, Changsha, ChinaSchool of Minerals Processing and Bioengineering, Central South University, Changsha, ChinaSchool of Minerals Processing and Bioengineering, Central South University, Changsha, ChinaSchool of Minerals Processing and Bioengineering, Central South University, Changsha, ChinaState Key Laboratory of Microbial Resources, Institute of Microbiology, Chinese Academy of Sciences, Beijing, ChinaState Key Laboratory of Microbial Resources, Institute of Microbiology, Chinese Academy of Sciences, Beijing, ChinaState Key Laboratory of Microbial Resources, Institute of Microbiology, Chinese Academy of Sciences, Beijing, ChinaCollege of Zijin Mining, Fuzhou University, Fuzhou, Fujian, ChinaDepartment of Environmental Microbiology and Biotechnology, Institute of Microbiology, Faculty of Biology, University of Warsaw, Warsaw, PolandDepartment of Environmental Microbiology and Biotechnology, Institute of Microbiology, Faculty of Biology, University of Warsaw, Warsaw, PolandSchool of Minerals Processing and Bioengineering, Central South University, Changsha, ChinaHunan Tobacco Science Institute, Changsha, China306 Geological Prospecting Party, Hunan Bureau of Geology and Mineral Exploration and Development, Changsha, China306 Geological Prospecting Party, Hunan Bureau of Geology and Mineral Exploration and Development, Changsha, ChinaState Key Laboratory of Microbial Resources, Institute of Microbiology, Chinese Academy of Sciences, Beijing, ChinaSchool of Minerals Processing and Bioengineering, Central South University, Changsha, ChinaABSTRACT DPANN is known as highly diverse, globally widespread, and mostly ectosymbiotic archaeal superphylum. However, this group of archaea was overlooked for a long time, and there were limited in-depth studies reported. In this investigation, 41 metagenome-assembled genomes (MAGs) belonging to the DPANN superphylum were recovered (18 MAGs had average nucleotide identity [ANI] values of <95% and a percentage of conserved proteins [POCP] of >50%, while 14 MAGs showed a POCP of <50%), which were analyzed comparatively with 515 other published DPANN genomes. Mismatches to known 16S rRNA gene primers were identified among 16S rRNA genes of DPANN archaea. Numbers of gene families lost (mostly related to energy and amino acid metabolism) were over three times greater than those gained in the evolution of DPANN archaea. Lateral gene transfer (LGT; ∼45.5% was cross-domain) had facilitated niche adaption of the DPANN archaea, ensuring a delicate equilibrium of streamlined genomes with efficient niche-adaptive strategies. For instance, LGT-derived cytochrome bd ubiquinol oxidase and arginine deiminase in the genomes of “Candidatus Micrarchaeota” could help them better adapt to aerobic acidic mine drainage habitats. In addition, most DPANN archaea acquired enzymes for biosynthesis of extracellular polymeric substances (EPS) and transketolase/transaldolase for the pentose phosphate pathway from Bacteria. IMPORTANCE 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. However, the DPANN superphylum still contains a vast genetic novelty and diversity that need to be explored. Comprehensively comparative genomic analysis on the DPANN superphylum was performed in this study, with an attempt to illuminate its metabolic potential, ecological distribution and evolutionary history. Many interphylum differences within the DPANN superphylum were found. For example, Altiarchaeota had the biggest genome among DPANN phyla, possessing many pathways missing in other phyla, such as formaldehyde assimilation and the Wood-Ljungdahl pathway. In addition, LGT acted as an important force to provide DPANN archaeal genetic flexibility that permitted the occupation of diverse niches. This study has advanced our understanding of the diversity and genome evolution of archaea.https://journals.asm.org/doi/10.1128/mSystems.00602-21DPANN superphylumevolutiongenome reductionlateral gene transfercomparative genomics |