Chemosynthetic symbionts of marine invertebrate animals are capable of nitrogen fixation

Jillian M Petersen; Anna Kemper; Harald Gruber-Vodicka; Ulisse Cardini; Matthijs van der Geest; Manuel Kleiner; Silvia Bulgheresi; Marc Mußmann; Craig Herbold; Brandon K B Seah; Chakkiath Paul Antony; Dan Liu; Alexandra Belitz; Miriam Weber

doi:10.1038/nmicrobiol.2016.195

Chemosynthetic symbionts of marine invertebrate animals are capable of nitrogen fixation

Jillian M Petersen (Corresponding author)
, Anna Kemper
, Harald Gruber-Vodicka
, Ulisse Cardini
, Matthijs van der Geest
, Manuel Kleiner
, Silvia Bulgheresi
, Marc Mußmann
, Craig Herbold
, Brandon K B Seah
, Chakkiath Paul Antony
, Dan Liu
, Alexandra Belitz
, Miriam Weber

Publications: Contribution to journal › Article › Peer Reviewed

Abstract

Chemosynthetic symbioses are partnerships between invertebrate animals and chemosynthetic bacteria. The latter are the
primary producers, providing most of the organic carbon needed for the animal host’s nutrition. We sequenced genomes
of the chemosynthetic symbionts from the lucinid bivalve Loripes lucinalis and the stilbonematid nematode Laxus oneistus.
The symbionts of both host species encoded nitrogen fixation genes. This is remarkable as no marine chemosynthetic
symbiont was previously known to be capable of nitrogen fixation. We detected nitrogenase expression by the symbionts
of lucinid clams at the transcriptomic and proteomic level. Mean stable nitrogen isotope values of Loripes lucinalis were
within the range expected for fixed atmospheric nitrogen, further suggesting active nitrogen fixation by the symbionts.
The ability to fix nitrogen may be widespread among chemosynthetic symbioses in oligotrophic habitats, where nitrogen
availability often limits primary productivity.

Original language	English
Article number	16195
Number of pages	11
Journal	Nature Microbiology
Volume	2
Issue number	1
DOIs	https://doi.org/10.1038/nmicrobiol.2016.195 https://doi.org/10.1038/s41564-018-0196-5
Publication status	Published - 24 Oct 2016

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

SDG 14 Life Below Water

Austrian Fields of Science 2012

106005 Bioinformatics
106026 Ecosystem research
106022 Microbiology
106021 Marine biology

Keywords

BIOGEOCHEMISTRY
microbial ecology
symbiosis
Water Microbiology
ENERGY
CARBON
ENDOSYMBIONTS
SHOTGUN PROTEOMICS
BACTERIAL
CHEMOAUTOTROPHY
ALIGNMENT
N-2 FIXATION
NIFH SEQUENCES
LUCINIDAE BIVALVIA

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Petersen, J. M., Kemper, A., Gruber-Vodicka, H., Cardini, U., van der Geest, M., Kleiner, M., Bulgheresi, S., Mußmann, M., Herbold, C., Seah, B. K. B., Antony, C. P., Liu, D., Belitz, A., & Weber, M. (2016). Chemosynthetic symbionts of marine invertebrate animals are capable of nitrogen fixation. Nature Microbiology, 2(1), Article 16195. https://doi.org/10.1038/nmicrobiol.2016.195, https://doi.org/10.1038/s41564-018-0196-5

@article{4739866d1c024d33a097d0d6ed439de6,

title = "Chemosynthetic symbionts of marine invertebrate animals are capable of nitrogen fixation",

abstract = "Chemosynthetic symbioses are partnerships between invertebrate animals and chemosynthetic bacteria. The latter are the primary producers, providing most of the organic carbon needed for the animal host{\textquoteright}s nutrition. We sequenced genomes of the chemosynthetic symbionts from the lucinid bivalve Loripes lucinalis and the stilbonematid nematode Laxus oneistus. The symbionts of both host species encoded nitrogen fixation genes. This is remarkable as no marine chemosynthetic symbiont was previously known to be capable of nitrogen fixation. We detected nitrogenase expression by the symbionts of lucinid clams at the transcriptomic and proteomic level. Mean stable nitrogen isotope values of Loripes lucinalis were within the range expected for fixed atmospheric nitrogen, further suggesting active nitrogen fixation by the symbionts. The ability to fix nitrogen may be widespread among chemosynthetic symbioses in oligotrophic habitats, where nitrogen availability often limits primary productivity.",

keywords = "BIOGEOCHEMISTRY, microbial ecology, symbiosis, Water Microbiology, ENERGY, CARBON, ENDOSYMBIONTS, SHOTGUN PROTEOMICS, BACTERIAL, CHEMOAUTOTROPHY, ALIGNMENT, N-2 FIXATION, NIFH SEQUENCES, LUCINIDAE BIVALVIA",

author = "Petersen, \{Jillian M\} and Anna Kemper and Harald Gruber-Vodicka and Ulisse Cardini and \{van der Geest\}, Matthijs and Manuel Kleiner and Silvia Bulgheresi and Marc Mu{\ss}mann and Craig Herbold and Seah, \{Brandon K B\} and Antony, \{Chakkiath Paul\} and Dan Liu and Alexandra Belitz and Miriam Weber",

note = "Correction to: Nature Microbiology https://doi.org/10.1038/nmicrobiol.2016.195, published online 24 October 2016. In this Article, the completeness and number of contigs for draft genomes from two individuals of Laxus oneistus are incorrect in the main text, although the correct information is included in Table 1. The original and corrected versions of the relevant sentence are shown in the correction notice. Original sentence: Those from two individuals of L. oneistus (Ca. Thiosymbion oneisti A–B) were 86.75 and 89.11\% complete at sizes of 3.66 and 3.51 Mb on 183 and 193 contigs (Table 1). Corrected sentence: Those from two individuals of L. oneistus (Ca. Thiosymbion oneisti A–B) were 96.63 and 96.07\% complete at sizes of 4.44 and 4.33 Mb on 2,026 and 1,891 contigs (Table 1).",

year = "2016",

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doi = "10.1038/nmicrobiol.2016.195",

language = "English",

volume = "2",

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issn = "2058-5276",

publisher = "NATURE PUBLISHING GROUP",

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}

Petersen, JM, Kemper, A, Gruber-Vodicka, H, Cardini, U, van der Geest, M, Kleiner, M, Bulgheresi, S , Mußmann, M, Herbold, C, Seah, BKB, Antony, CP, Liu, D, Belitz, A & Weber, M 2016, 'Chemosynthetic symbionts of marine invertebrate animals are capable of nitrogen fixation', Nature Microbiology, vol. 2, no. 1, 16195. https://doi.org/10.1038/nmicrobiol.2016.195, https://doi.org/10.1038/s41564-018-0196-5

TY - JOUR

T1 - Chemosynthetic symbionts of marine invertebrate animals are capable of nitrogen fixation

AU - Petersen, Jillian M

AU - Kemper, Anna

AU - Gruber-Vodicka, Harald

AU - Cardini, Ulisse

AU - van der Geest, Matthijs

AU - Kleiner, Manuel

AU - Bulgheresi, Silvia

AU - Mußmann, Marc

AU - Herbold, Craig

AU - Seah, Brandon K B

AU - Antony, Chakkiath Paul

AU - Liu, Dan

AU - Belitz, Alexandra

AU - Weber, Miriam

N1 - Correction to: Nature Microbiology https://doi.org/10.1038/nmicrobiol.2016.195, published online 24 October 2016. In this Article, the completeness and number of contigs for draft genomes from two individuals of Laxus oneistus are incorrect in the main text, although the correct information is included in Table 1. The original and corrected versions of the relevant sentence are shown in the correction notice. Original sentence: Those from two individuals of L. oneistus (Ca. Thiosymbion oneisti A–B) were 86.75 and 89.11% complete at sizes of 3.66 and 3.51 Mb on 183 and 193 contigs (Table 1). Corrected sentence: Those from two individuals of L. oneistus (Ca. Thiosymbion oneisti A–B) were 96.63 and 96.07% complete at sizes of 4.44 and 4.33 Mb on 2,026 and 1,891 contigs (Table 1).

PY - 2016/10/24

Y1 - 2016/10/24

N2 - Chemosynthetic symbioses are partnerships between invertebrate animals and chemosynthetic bacteria. The latter are the primary producers, providing most of the organic carbon needed for the animal host’s nutrition. We sequenced genomes of the chemosynthetic symbionts from the lucinid bivalve Loripes lucinalis and the stilbonematid nematode Laxus oneistus. The symbionts of both host species encoded nitrogen fixation genes. This is remarkable as no marine chemosynthetic symbiont was previously known to be capable of nitrogen fixation. We detected nitrogenase expression by the symbionts of lucinid clams at the transcriptomic and proteomic level. Mean stable nitrogen isotope values of Loripes lucinalis were within the range expected for fixed atmospheric nitrogen, further suggesting active nitrogen fixation by the symbionts. The ability to fix nitrogen may be widespread among chemosynthetic symbioses in oligotrophic habitats, where nitrogen availability often limits primary productivity.

AB - Chemosynthetic symbioses are partnerships between invertebrate animals and chemosynthetic bacteria. The latter are the primary producers, providing most of the organic carbon needed for the animal host’s nutrition. We sequenced genomes of the chemosynthetic symbionts from the lucinid bivalve Loripes lucinalis and the stilbonematid nematode Laxus oneistus. The symbionts of both host species encoded nitrogen fixation genes. This is remarkable as no marine chemosynthetic symbiont was previously known to be capable of nitrogen fixation. We detected nitrogenase expression by the symbionts of lucinid clams at the transcriptomic and proteomic level. Mean stable nitrogen isotope values of Loripes lucinalis were within the range expected for fixed atmospheric nitrogen, further suggesting active nitrogen fixation by the symbionts. The ability to fix nitrogen may be widespread among chemosynthetic symbioses in oligotrophic habitats, where nitrogen availability often limits primary productivity.

KW - BIOGEOCHEMISTRY

KW - microbial ecology

KW - symbiosis

KW - Water Microbiology

KW - ENERGY

KW - CARBON

KW - ENDOSYMBIONTS

KW - SHOTGUN PROTEOMICS

KW - BACTERIAL

KW - CHEMOAUTOTROPHY

KW - ALIGNMENT

KW - N-2 FIXATION

KW - NIFH SEQUENCES

KW - LUCINIDAE BIVALVIA

UR - https://www.scopus.com/pages/publications/84992313107

U2 - 10.1038/nmicrobiol.2016.195

DO - 10.1038/nmicrobiol.2016.195

M3 - Article

C2 - 27775707

SN - 2058-5276

VL - 2

JO - Nature Microbiology

JF - Nature Microbiology

IS - 1

M1 - 16195

ER -

Chemosynthetic symbionts of marine invertebrate animals are capable of nitrogen fixation

Abstract

UN SDGs

Austrian Fields of Science 2012

Keywords

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