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Chemotaxis may assist marine heterotrophic bacterial diazotrophs to find microzones suitable for N2 fixation in the pelagic ocean

Abstract

Heterotrophic bacterial diazotrophs (HBDs) are ubiquitous in the pelagic ocean, where they have been predicted to carry out the anaerobic process of nitrogen fixation within low-oxygen microenvironments associated with marine pelagic particles. However, the mechanisms enabling particle colonization by HBDs are unknown. We hypothesized that HBDs use chemotaxis to locate and colonize suitable microenvironments, and showed that a cultivated marine HBD is chemotactic toward amino acids and phytoplankton-derived DOM. Using an in situ chemotaxis assay, we also discovered that diverse HBDs at a coastal site are motile and chemotactic toward DOM from various phytoplankton taxa and, indeed, that the proportion of diazotrophs was up to seven times higher among the motile fraction of the bacterial community compared to the bulk seawater community. Finally, three of four HBD isolates and 16 of 17 HBD metagenome assembled genomes, recovered from major ocean basins and locations along the Australian coast, each encoded >85% of proteins affiliated with the bacterial chemotaxis pathway. These results document the widespread capacity for chemotaxis in diverse and globally relevant marine HBDs. We suggest that HBDs could use chemotaxis to seek out and colonize low-oxygen microenvironments suitable for nitrogen fixation, such as those formed on marine particles. Chemotaxis in HBDs could therefore affect marine nitrogen and carbon biogeochemistry by facilitating nitrogen fixation within otherwise oxic waters, while also altering particle degradation and the efficiency of the biological pump.

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Fig. 1: Chemotaxis by Pseudomonas stutzeri.
Fig. 2: Diazotrophs in a natural bacterioplankton community are motile and capable of performing chemotaxis.
Fig. 3: Diversity and composition of motile and chemotactic diazotrophs.
Fig. 4: Chemotaxis is a prevailing phenotype in HBDs.

Data availability

The raw FASTQ read files were deposited in the Sequence Read Archive (SRA) (accession number: PRJNA639602). The AMI MAGs used in this work are deposited on figshare (https://doi.org/10.6084/m9.figshare.13292774). We have also made publicly available (1) the metagenomic reads that mapped to nifH (https://doi.org/10.6084/m9.figshare.13027634), (2) the data used to generate the phylogenetic placement of metagenomic reads including nifH reference and environmental sequences used to construct the phylogenetic tree, collection of metagenomic reads (>100 bps), and the output from the phylogenetic placement (https://doi.org/10.6084/m9.figshare.13027706), as well as (3) seed protein alignments (https://doi.org/10.6084/m9.figshare.13027760) and (4) the custom HMMs (https://doi.org/10.6084/m9.figshare.13027781) for each of the investigated proteins included in the genetic survey of motility and chemotaxis.

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Acknowledgements

The authors acknowledge the contribution of the Marine Microbes consortium and the Tara Oceans consortium in the generation of data used in this publication. The Marine Microbes Initiative was supported by funding from Bioplatforms Australia and the Integrated Marine Observing System (IMOS) through the Australian Government National Collaborative Research Infrastructure Strategy (NCRIS) in partnership with the Australian research community. The authors thank H. Price for assisting with the TOC analysis. We acknowledge use of computing resources at the core facility for biocomputing at the Department of Biology, University of Copenhagen.

Funding

This work was supported by the Danish Council for Independent Research (6108-00013) awarded to LR and Gordon & Betty Moore Foundation Grant (GBMF3801) awarded to JRS, RS, GWT, and PH.

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SH, JBR, GWT, PH, RS, JRS, and LR designed the experiments. SH and JBR performed the experiments. JBR and DHP generated and analyzed the complete metagenomic dataset. SH conducted the nifH specific analysis. The genomic survey was carried out by SH and MO. SH, JBR, JRS, and LR wrote the manuscript. All authors edited the manuscript before submission.

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Correspondence to Lasse Riemann.

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Hallstrøm, S., Raina, JB., Ostrowski, M. et al. Chemotaxis may assist marine heterotrophic bacterial diazotrophs to find microzones suitable for N2 fixation in the pelagic ocean. ISME J (2022). https://doi.org/10.1038/s41396-022-01299-4

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