Rich microbial and depolymerising diversity in Antarctic krill gut

ABSTRACT With almost a quadrillion individuals, the Antarctic krill processes five million tons of organic carbon every day during austral summer. This high carbon flux requires a broad range of hydrolytic enzymes to decompose the diverse food-derived biopolymers. While krill itself possesses numero...

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Published in:Microbiology Spectrum
Main Authors: Möller, Lars, Vainshtein, Yevhen, Meyer, Bettina, Neidhardt, John, Eren, A. Murat, Sohn, Kai, Rabus, Ralf
Other Authors: Kormas, Konstantinos Aristomenis, Bundesministerium für Bildung und Forschung
Format: Article in Journal/Newspaper
Language:English
Published: American Society for Microbiology 2024
Subjects:
Online Access:http://dx.doi.org/10.1128/spectrum.04035-23
https://journals.asm.org/doi/pdf/10.1128/spectrum.04035-23
id crasmicro:10.1128/spectrum.04035-23
record_format openpolar
spelling crasmicro:10.1128/spectrum.04035-23 2024-04-28T08:01:12+00:00 Rich microbial and depolymerising diversity in Antarctic krill gut Möller, Lars Vainshtein, Yevhen Meyer, Bettina Neidhardt, John Eren, A. Murat Sohn, Kai Rabus, Ralf Kormas, Konstantinos Aristomenis Bundesministerium für Bildung und Forschung 2024 http://dx.doi.org/10.1128/spectrum.04035-23 https://journals.asm.org/doi/pdf/10.1128/spectrum.04035-23 en eng American Society for Microbiology https://creativecommons.org/licenses/by/4.0/ https://journals.asm.org/non-commercial-tdm-license Microbiology Spectrum volume 12, issue 4 ISSN 2165-0497 Infectious Diseases Cell Biology Microbiology (medical) Genetics General Immunology and Microbiology Ecology Physiology journal-article 2024 crasmicro https://doi.org/10.1128/spectrum.04035-23 2024-04-09T06:52:37Z ABSTRACT With almost a quadrillion individuals, the Antarctic krill processes five million tons of organic carbon every day during austral summer. This high carbon flux requires a broad range of hydrolytic enzymes to decompose the diverse food-derived biopolymers. While krill itself possesses numerous such enzymes, it is unclear, to what extent the endogenous microbiota contribute to the hydrolytic potential of the gut environment. Here we applied amplicon sequencing, shotgun metagenomics, cultivation, and physiological assays to characterize the krill gut microbiota. The broad bacterial diversity (273 families, 919 genera, and 2,309 species) also included a complex potentially anaerobic sub-community. Plate-based assays with 198 isolated pure cultures revealed widespread capacities to utilize lipids (e.g., tributyrin), followed by proteins (casein) and to a lesser extent by polysaccharides (e.g., alginate and chitin). While most isolates affiliated with the genera Pseudoalteromonas and Psychrobacter , also Rubritalea spp. (Verrucomicrobia) were observed. The krill gut microbiota growing on marine broth agar plates possess 13,012 predicted hydrolyses; 15-fold more than previously predicted from a transcriptome-proteome compendium of krill. Cultivation-independent and -dependent approaches indicated members of the families Flavobacteriaceae and Pseudoalteromonadaceae to dominate the capacities for lipid/protein hydrolysis and to provide a plethora of carbohydrate-active enzymes, sulfatases, and laminarin- or porphyrin-depolymerizing hydrolases. Notably, also the potential to hydrolyze plastics such as polyethylene terephthalate and polylactatide was observed, affiliating mostly with Moraxellaceae. Overall, this study shows extensive microbial diversity in the krill gut, and suggests that the microbiota likely play a significant role in the nutrient acquisition of the krill by enriching its hydrolytic enzyme repertoire. IMPORTANCE The Antarctic krill ( Euphausia superba ) is a keystone species of the Antarctic ... Article in Journal/Newspaper Antarc* Antarctic Antarctic Krill Euphausia superba ASM Journals (American Society for Microbiology) Microbiology Spectrum
institution Open Polar
collection ASM Journals (American Society for Microbiology)
op_collection_id crasmicro
language English
topic Infectious Diseases
Cell Biology
Microbiology (medical)
Genetics
General Immunology and Microbiology
Ecology
Physiology
spellingShingle Infectious Diseases
Cell Biology
Microbiology (medical)
Genetics
General Immunology and Microbiology
Ecology
Physiology
Möller, Lars
Vainshtein, Yevhen
Meyer, Bettina
Neidhardt, John
Eren, A. Murat
Sohn, Kai
Rabus, Ralf
Rich microbial and depolymerising diversity in Antarctic krill gut
topic_facet Infectious Diseases
Cell Biology
Microbiology (medical)
Genetics
General Immunology and Microbiology
Ecology
Physiology
description ABSTRACT With almost a quadrillion individuals, the Antarctic krill processes five million tons of organic carbon every day during austral summer. This high carbon flux requires a broad range of hydrolytic enzymes to decompose the diverse food-derived biopolymers. While krill itself possesses numerous such enzymes, it is unclear, to what extent the endogenous microbiota contribute to the hydrolytic potential of the gut environment. Here we applied amplicon sequencing, shotgun metagenomics, cultivation, and physiological assays to characterize the krill gut microbiota. The broad bacterial diversity (273 families, 919 genera, and 2,309 species) also included a complex potentially anaerobic sub-community. Plate-based assays with 198 isolated pure cultures revealed widespread capacities to utilize lipids (e.g., tributyrin), followed by proteins (casein) and to a lesser extent by polysaccharides (e.g., alginate and chitin). While most isolates affiliated with the genera Pseudoalteromonas and Psychrobacter , also Rubritalea spp. (Verrucomicrobia) were observed. The krill gut microbiota growing on marine broth agar plates possess 13,012 predicted hydrolyses; 15-fold more than previously predicted from a transcriptome-proteome compendium of krill. Cultivation-independent and -dependent approaches indicated members of the families Flavobacteriaceae and Pseudoalteromonadaceae to dominate the capacities for lipid/protein hydrolysis and to provide a plethora of carbohydrate-active enzymes, sulfatases, and laminarin- or porphyrin-depolymerizing hydrolases. Notably, also the potential to hydrolyze plastics such as polyethylene terephthalate and polylactatide was observed, affiliating mostly with Moraxellaceae. Overall, this study shows extensive microbial diversity in the krill gut, and suggests that the microbiota likely play a significant role in the nutrient acquisition of the krill by enriching its hydrolytic enzyme repertoire. IMPORTANCE The Antarctic krill ( Euphausia superba ) is a keystone species of the Antarctic ...
author2 Kormas, Konstantinos Aristomenis
Bundesministerium für Bildung und Forschung
format Article in Journal/Newspaper
author Möller, Lars
Vainshtein, Yevhen
Meyer, Bettina
Neidhardt, John
Eren, A. Murat
Sohn, Kai
Rabus, Ralf
author_facet Möller, Lars
Vainshtein, Yevhen
Meyer, Bettina
Neidhardt, John
Eren, A. Murat
Sohn, Kai
Rabus, Ralf
author_sort Möller, Lars
title Rich microbial and depolymerising diversity in Antarctic krill gut
title_short Rich microbial and depolymerising diversity in Antarctic krill gut
title_full Rich microbial and depolymerising diversity in Antarctic krill gut
title_fullStr Rich microbial and depolymerising diversity in Antarctic krill gut
title_full_unstemmed Rich microbial and depolymerising diversity in Antarctic krill gut
title_sort rich microbial and depolymerising diversity in antarctic krill gut
publisher American Society for Microbiology
publishDate 2024
url http://dx.doi.org/10.1128/spectrum.04035-23
https://journals.asm.org/doi/pdf/10.1128/spectrum.04035-23
genre Antarc*
Antarctic
Antarctic Krill
Euphausia superba
genre_facet Antarc*
Antarctic
Antarctic Krill
Euphausia superba
op_source Microbiology Spectrum
volume 12, issue 4
ISSN 2165-0497
op_rights https://creativecommons.org/licenses/by/4.0/
https://journals.asm.org/non-commercial-tdm-license
op_doi https://doi.org/10.1128/spectrum.04035-23
container_title Microbiology Spectrum
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