Subgroup level differences of physiological activities in marine Lokiarchaeota

Xiuran Yin; Mingwei Cai; Yang Liu; Guowei Zhou; Tim Richter-Heitmann; David A. Aromokeye; Ajinkya C. Kulkarni; Rolf Nimzyk; Henrik Cullhed; Zhichao Zhou; Jie Pan; Yuchun Yang; Ji Dong Gu; Marcus Elvert; Meng Li; Michael W. Friedrich

doi:10.1038/s41396-020-00818-5

Subgroup level differences of physiological activities in marine Lokiarchaeota

Xiuran Yin, Mingwei Cai, Yang Liu, Guowei Zhou, Tim Richter-Heitmann, David A. Aromokeye, Ajinkya C. Kulkarni, Rolf Nimzyk, Henrik Cullhed, Zhichao Zhou, Jie Pan, Yuchun Yang, Ji Dong Gu, Marcus Elvert, Meng Li, Michael W. Friedrich^*

^*Corresponding author for this work

Research output: Contribution to journal › Article › peer-review

6 Scopus citations

Abstract

Asgard is a recently discovered archaeal superphylum, closely linked to the emergence of eukaryotes. Among Asgard archaea, Lokiarchaeota are abundant in marine sediments, but their in situ activities are largely unknown except for Candidatus ‘Prometheoarchaeum syntrophicum’. Here, we tracked the activity of Lokiarchaeota in incubations with Helgoland mud area sediments (North Sea) by stable isotope probing (SIP) with organic polymers, ¹³C-labelled inorganic carbon, fermentation intermediates and proteins. Within the active archaea, we detected members of the Lokiarchaeota class Loki-3, which appeared to mixotrophically participate in the degradation of lignin and humic acids while assimilating CO₂, or heterotrophically used lactate. In contrast, members of the Lokiarchaeota class Loki-2 utilized protein and inorganic carbon, and degraded bacterial biomass formed in incubations. Metagenomic analysis revealed pathways for lactate degradation, and involvement in aromatic compound degradation in Loki-3, while the less globally distributed Loki-2 instead rely on protein degradation. We conclude that Lokiarchaeotal subgroups vary in their metabolic capabilities despite overlaps in their genomic equipment, and suggest that these subgroups occupy different ecologic niches in marine sediments.

Original language	English
Pages (from-to)	848-861
Number of pages	14
Journal	ISME Journal
Volume	15
Issue number	3
DOIs	https://doi.org/10.1038/s41396-020-00818-5
State	Published - Mar 2021
Externally published	Yes

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10.1038/s41396-020-00818-5

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Yin, Xiuran ; Cai, Mingwei ; Liu, Yang ; Zhou, Guowei ; Richter-Heitmann, Tim ; Aromokeye, David A. ; Kulkarni, Ajinkya C. ; Nimzyk, Rolf ; Cullhed, Henrik ; Zhou, Zhichao ; Pan, Jie ; Yang, Yuchun ; Gu, Ji Dong ; Elvert, Marcus ; Li, Meng ; Friedrich, Michael W. / Subgroup level differences of physiological activities in marine Lokiarchaeota. In: ISME Journal. 2021 ; Vol. 15, No. 3. pp. 848-861.

@article{349c4429ba744212a2b53f4eb4a765ec,

title = "Subgroup level differences of physiological activities in marine Lokiarchaeota",

abstract = "Asgard is a recently discovered archaeal superphylum, closely linked to the emergence of eukaryotes. Among Asgard archaea, Lokiarchaeota are abundant in marine sediments, but their in situ activities are largely unknown except for Candidatus {\textquoteleft}Prometheoarchaeum syntrophicum{\textquoteright}. Here, we tracked the activity of Lokiarchaeota in incubations with Helgoland mud area sediments (North Sea) by stable isotope probing (SIP) with organic polymers, 13C-labelled inorganic carbon, fermentation intermediates and proteins. Within the active archaea, we detected members of the Lokiarchaeota class Loki-3, which appeared to mixotrophically participate in the degradation of lignin and humic acids while assimilating CO2, or heterotrophically used lactate. In contrast, members of the Lokiarchaeota class Loki-2 utilized protein and inorganic carbon, and degraded bacterial biomass formed in incubations. Metagenomic analysis revealed pathways for lactate degradation, and involvement in aromatic compound degradation in Loki-3, while the less globally distributed Loki-2 instead rely on protein degradation. We conclude that Lokiarchaeotal subgroups vary in their metabolic capabilities despite overlaps in their genomic equipment, and suggest that these subgroups occupy different ecologic niches in marine sediments.",

author = "Xiuran Yin and Mingwei Cai and Yang Liu and Guowei Zhou and Tim Richter-Heitmann and Aromokeye, {David A.} and Kulkarni, {Ajinkya C.} and Rolf Nimzyk and Henrik Cullhed and Zhichao Zhou and Jie Pan and Yuchun Yang and Gu, {Ji Dong} and Marcus Elvert and Meng Li and Friedrich, {Michael W.}",

note = "Publisher Copyright: {\textcopyright} 2020, The Author(s).",

year = "2021",

month = mar,

doi = "10.1038/s41396-020-00818-5",

language = "英语",

volume = "15",

pages = "848--861",

journal = "ISME Journal",

issn = "1751-7362",

publisher = "Nature Publishing Group",

number = "3",

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Subgroup level differences of physiological activities in marine Lokiarchaeota. / Yin, Xiuran; Cai, Mingwei; Liu, Yang; Zhou, Guowei; Richter-Heitmann, Tim; Aromokeye, David A.; Kulkarni, Ajinkya C.; Nimzyk, Rolf; Cullhed, Henrik; Zhou, Zhichao; Pan, Jie; Yang, Yuchun; Gu, Ji Dong; Elvert, Marcus; Li, Meng; Friedrich, Michael W.

In: ISME Journal, Vol. 15, No. 3, 03.2021, p. 848-861.

Research output: Contribution to journal › Article › peer-review

TY - JOUR

T1 - Subgroup level differences of physiological activities in marine Lokiarchaeota

AU - Yin, Xiuran

AU - Cai, Mingwei

AU - Liu, Yang

AU - Zhou, Guowei

AU - Richter-Heitmann, Tim

AU - Aromokeye, David A.

AU - Kulkarni, Ajinkya C.

AU - Nimzyk, Rolf

AU - Cullhed, Henrik

AU - Zhou, Zhichao

AU - Pan, Jie

AU - Yang, Yuchun

AU - Gu, Ji Dong

AU - Elvert, Marcus

AU - Li, Meng

AU - Friedrich, Michael W.

PY - 2021/3

Y1 - 2021/3

N2 - Asgard is a recently discovered archaeal superphylum, closely linked to the emergence of eukaryotes. Among Asgard archaea, Lokiarchaeota are abundant in marine sediments, but their in situ activities are largely unknown except for Candidatus ‘Prometheoarchaeum syntrophicum’. Here, we tracked the activity of Lokiarchaeota in incubations with Helgoland mud area sediments (North Sea) by stable isotope probing (SIP) with organic polymers, 13C-labelled inorganic carbon, fermentation intermediates and proteins. Within the active archaea, we detected members of the Lokiarchaeota class Loki-3, which appeared to mixotrophically participate in the degradation of lignin and humic acids while assimilating CO2, or heterotrophically used lactate. In contrast, members of the Lokiarchaeota class Loki-2 utilized protein and inorganic carbon, and degraded bacterial biomass formed in incubations. Metagenomic analysis revealed pathways for lactate degradation, and involvement in aromatic compound degradation in Loki-3, while the less globally distributed Loki-2 instead rely on protein degradation. We conclude that Lokiarchaeotal subgroups vary in their metabolic capabilities despite overlaps in their genomic equipment, and suggest that these subgroups occupy different ecologic niches in marine sediments.

AB - Asgard is a recently discovered archaeal superphylum, closely linked to the emergence of eukaryotes. Among Asgard archaea, Lokiarchaeota are abundant in marine sediments, but their in situ activities are largely unknown except for Candidatus ‘Prometheoarchaeum syntrophicum’. Here, we tracked the activity of Lokiarchaeota in incubations with Helgoland mud area sediments (North Sea) by stable isotope probing (SIP) with organic polymers, 13C-labelled inorganic carbon, fermentation intermediates and proteins. Within the active archaea, we detected members of the Lokiarchaeota class Loki-3, which appeared to mixotrophically participate in the degradation of lignin and humic acids while assimilating CO2, or heterotrophically used lactate. In contrast, members of the Lokiarchaeota class Loki-2 utilized protein and inorganic carbon, and degraded bacterial biomass formed in incubations. Metagenomic analysis revealed pathways for lactate degradation, and involvement in aromatic compound degradation in Loki-3, while the less globally distributed Loki-2 instead rely on protein degradation. We conclude that Lokiarchaeotal subgroups vary in their metabolic capabilities despite overlaps in their genomic equipment, and suggest that these subgroups occupy different ecologic niches in marine sediments.

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U2 - 10.1038/s41396-020-00818-5

DO - 10.1038/s41396-020-00818-5

M3 - 文章

C2 - 33149207

AN - SCOPUS:85094940179

VL - 15

SP - 848

EP - 861

JO - ISME Journal

JF - ISME Journal

SN - 1751-7362

IS - 3

ER -

Subgroup level differences of physiological activities in marine Lokiarchaeota

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