Dataset Information

Chemotaxis shapes the microscale organization of the ocean’s microbiome

ABSTRACT:

The capacity of planktonic marine microorganisms to actively seek out and exploit microscale chemical hotspots has been widely theorized to affect ocean-basin scale biogeochemistry, but has never been examined comprehensively in situ among natural microbial communities. Here, using a field-based microfluidic platform to quantify the behavioural responses of marine bacteria and archaea, we observed significant levels of chemotaxis towards microscale hotspots of phytoplankton-derived dissolved organic matter (DOM) at a coastal field site across multiple deployments, spanning several months. Microscale metagenomics revealed that a wide diversity of marine prokaryotes, spanning 27 bacterial and 2 archaeal phyla, displayed chemotaxis towards microscale patches of DOM derived from 10 globally distributed phytoplankton species. The distinct DOM composition of each phytoplankton species attracted phylogenetically and functionally discrete populations of bacteria and archaea, with 54% of chemotactic prokaryotes displaying highly specific responses to the DOM derived from only one or two phytoplankton species. Prokaryotes exhibiting chemotaxis towards phytoplankton-derived compounds were significantly enriched in the capacity to transport and metabolize specific phytoplankton-derived chemicals, and displayed enrichment in functions conducive to symbiotic relationships, including genes involved in the production of siderophores, B vitamins and growth-promoting hormones. Our findings demonstrate that the swimming behaviour of natural prokaryotic assemblages is governed by specific chemical cues, which dictate important biogeochemical transformation processes and the establishment of ecological interactions that structure the base of the marine food web.

INSTRUMENT(S): Gas Chromatography MS - positive

SUBMITTER: Jean-Baptiste Raina

PROVIDER: MTBLS1980 | MetaboLights | 2022-02-15

REPOSITORIES: MetaboLights

ACCESS DATA

Publications

Chemotaxis shapes the microscale organization of the ocean's microbiome.

Raina Jean-Baptiste JB Lambert Bennett S BS Parks Donovan H DH Rinke Christian C Siboni Nachshon N Bramucci Anna A Ostrowski Martin M Signal Brandon B Lutz Adrian A Mendis Himasha H Rubino Francesco F Fernandez Vicente I VI Stocker Roman R Hugenholtz Philip P Tyson Gene W GW Seymour Justin R JR

Nature 20220420 7908

PMID: 35444277

Similar Datasets

Project description:Marine phytoplankton are a diverse group of photoautotrophic organisms and key mediators in the global carbon cycle. Phytoplankton physiology and biomass accumulation are closely tied to mixed layer depth, but the intracellular metabolic pathways activated in response to changing mixed layer depths remain unexplored. Here, metatranscriptomics was used to characterize the phytoplankton community response to a mixed layer shallowing from 233 meters to 5 meters over the course of two days during the late spring in the Northwest Atlantic. Most phytoplankton genera downregulated core photosynthesis, carbon storage, and carbon fixation genes as the system transitioned from a deep to a shallow mixed layer and shifted towards catabolism of stored carbon ic pathways supportive of rapid cell growth. In contrast, phytoplankton genera exhibited divergent transcriptional strategies for photosystem light harvesting complex genes during this transition. Active infection, taken as the ratio of virus to host transcripts, increased in the Bacillariophyta (diatom) phylum and decreased in the Chlorophyta (green algae) phylum upon mixed layer shallowing. A conceptual model is proposed to provide ecophysiological context for our findings, in which light limitation during deep mixing induces populations into a transcriptional state which maximizes interrupts the oscillating levels of transcripts related to photosynthesis, carbon storage, and carbon fixation found in shallow mixed layers with relatively higher growth rates. We propose that upon sensing high light levels during mixed layer shallowing, phytoplankton resume diel oscillation of core sets of genes enabling photoprotection, biosynthesis and cell replication. Our findings highlight the shared and unique transcriptional response strategies within phytoplankton communities acclimating to the dynamic light environment associated with transient deep mixing and shallowing events during the annual North Atlantic bloom.

Project description:Microbial photoautotroph-heterotroph interactions underlie marine food webs and shape ecosystem diversity and structure in upper ocean environments. However, the high complexity of in situ ecosystems renders it difficult to study these interactions. Two-member co-culture systems of picocyanobacteria and single heterotrophic bacterial strains have been thoroughly investigated. However, in situ interactions comprise far more diverse heterotrophic bacterial associations with single photoautotrophic organisms. Here, bacterial community composition, lifestyle preference, and genomic- and proteomic-level metabolic characteristics were investigated for an open ocean Synechococcus ecotype and its associated heterotrophs over 91 days of co-cultivation. The associated heterotrophic bacterial assembly mostly constituted five classes including Flavobacteria, Bacteroidetes, Phycisphaerae, Gammaproteobacteria, and Alphaproteobacteria. The seven most abundant taxa/genera comprised >90% of the total heterotrophic bacterial community, and five of these displayed distinct lifestyle preferences (free-living or attached) and responses to Synechococcus growth phases. Six high-quality genomes from the co-culture system were reconstructed inclusive of Synechococcus and the five dominant heterotrophic bacterial populations. The only primary producer of the co-culture system, Synechococcus, displayed metabolic processes primarily involved in inorganic nutrient uptake, photosynthesis, and organic matter biosynthesis and release. Two of the flavobacterial populations, Muricauda and Winogradskyella, and an SM1A02 population, displayed preferences for initial degradation of complex compounds and biopolymers, as evinced by high abundances of TBDT, glycoside hydrolase, and peptidases proteins. In contrast, the alphaproteobacterium Oricola sp. population mainly utilized low molecular weight DOM, including Flavobacteria metabolism byproducts, through ABC, TRAP, and TTT transport systems. Polysaccharide-utilization loci present in the flavobacterial genomes encoded similar trans-membrane protein complexes as Sus/cellulosome and may influence their lifestyle preferences and close associations with phytoplankton. The heterotrophic bacterial populations exhibited complementary mechanisms for degrading Synechococcus-derived organic matter and driving nutrient cycling. In addition to nutrient exchange, removal of reactive oxygen species and vitamin trafficking also contributed to the maintenance of the Synechococcus / heterotroph co-culture system and the interactions shaping the system.

Dataset Information

Chemotaxis shapes the microscale organization of the ocean’s microbiome

Publications

Chemotaxis shapes the microscale organization of the ocean's microbiome.

Similar Datasets

OmicsDI is part of the ELIXIR infrastructure