The dynamic trophic architecture of open-ocean protist communities revealed through machine-guided metatranscriptomics

Abstract

Intricate networks of single-celled eukaryotes (protists) dominate carbon flow in the ocean. Their growth, demise, and interactions with other microorganisms drive the fluxes of biogeochemical elements through marine ecosystems. Mixotrophic protists are capable of both photosynthesis and ingestion of prey and are dominant components of open-ocean planktonic communities. Yet, the role of mixotrophs in elemental cycling is obscured by their capacity to act as primary producers or heterotrophic consumers depending on factors that remain largely uncharacterized. Here we introduce a machine learning model that can predict the in situ nutritional mode of aquatic protists based on their patterns of gene expression. This approach leverages a public collection of protist transcriptomes as a training set to identify a subset of gene families whose transcriptional profiles predict trophic status. We applied our model to nearly 100 metatranscriptomes obtained during two oceanographic cruises in the North Pacific and found community-level and population-specific evidence that abundant open-ocean mixotrophic populations shift their predominant mode of nutrient and carbon acquisition in response to natural gradients in nutrient supply and sea surface temperature. In addition, metatranscriptomic data from ship-board incubation experiments revealed that abundant mixotrophic prymnesiophytes from the oligotrophic North Pacific subtropical gyre rapidly remodelled their transcriptome to enhance photosynthesis when supplied with limiting nutrients. Coupling the technique introduced here with experiments designed to reveal the mechanisms driving mixotroph physiology is a promising approach for understanding the ecology of mixotrophic populations in the natural environment.Significance statementMixotrophy is a ubiquitous nutritional strategy in marine ecosystems. Although our understanding of the distribution and abundance of mixotrophic plankton has improved significantly, the functional roles of mixotrophs are difficult to pinpoint, as mixotroph nutritional strategies are flexible and form a continuum between heterotrophy and phototrophy. We employ a machine learning-driven metatranscriptomic technique to assess the nutritional strategies of abundant planktonic populations in situ and demonstrate that mixotrophic populations play varying functional roles along physico-chemical gradients in the North Pacific Ocean, revealing a degree of physiological plasticity unique to aquatic mixotrophs. Our results highlight mechanisms that may dictate the flow of biogeochemical elements and the ecology of the North Pacific Ocean, one of the largest biogeographical provinces on Earth.

Eukaryotic genomes from a global metagenomic dataset illuminate trophic modes and biogeography of ocean plankton

“…ML approaches have been recently shown to be capable of accurate functional prediction and cell type annotation using genetic input, in particular for cancer cell prediction (Shipp et al, 2002; Bashiri et al, 2017; Tabl et al, 2019), and functional gene and phenotype prediction in plants (Mahood et al, 2020). Recently, these approaches have been applied to culture and environmental transcriptomic data to predict trophic mode using currently available trophy annotations (Lambert et al, 2021; Burns et al, 2018; Jimenez et al, 2021). Here, we apply an independent machine learning model to the eukaryotic TOPAZ MAGs to predict each organisms’ capacity for various metabolisms.…”

A system-level view on the function of natural eukaryotic biomes through taxonomically resolved metabolic pathway profiling

“…To this end, the application of nextgeneration sequencing (NGS) technologies has fueled the use of global gene expression profiles from environmental samples as an approximation of ecological function in microbial communities [9]. The approach has become a standard procedure to interrogate the physiological status of a variety of microbiomes from disparate ecosystems, such as terrestrial [10,11], aquatic [12][13][14] and human gut environments [15,16].…”

“…Most meta-omics studies of the marine microbiome have so far placed emphasis on the reconstruction of extensive gene catalogs and the delineation of protein functional clusters from a large set of samples collected across different oceanic provinces [33][34][35]. Notably, such sequence catalogs have proven effective as a general framework for studying planktonic ecosystems, including the association between gene sequence diversity and expression patterns with ecoregions, metabolic processes and trophic modes [13,14,25,26]. Although these bioinformatic approaches have greatly advanced our understanding of planktonic ecosystems, novel bioinformatics tools facilitating a systems biology analysis of meta-omics datasets are needed for e.g.…”

Diel-Regulated Transcriptional Cascades of Microbial Eukaryotes in the North Pacific Subtropical Gyre

“…The strictly heterotrophic (zooplankton) component of the protist community is dominated by the Alveolata supergroup (including dinoflagellates), as well as stramenopiles and Rhizaria ( Rii, 2016 ; Hu et al, 2018 ). Many eukaryotic lineages within the NPSG have mixotrophic life strategies, adjusting their relative balance of photosynthesis and phagotrophy to changing light and nutrient conditions ( Mitra et al, 2016 ; Lambert et al, 2021 ). In addition, mixotrophs can be distinguished between constitutive (vertical inheritance of plastids) and non-constitutive (kleptoplastic, or acquisition of plastids from prey) ( Mitra et al, 2016 ).…”

“…Members of haptophyte, ochrophyte, and dinoflagellate lineages are constitutive mixotrophs ( Faure et al, 2019 ), with evidence that they can graze on picocyanobacteria in the NPSG ( Frias-Lopez et al, 2009 ). In the well-lit and low nutrient conditions of the NPSG, mixotrophy may be advantageous ( Rothhaupt, 1996 ), and the gene family abundance profiles of many environmental protist species suggest widespread mixotrophy ( Lambert et al, 2021 ). Some ciliates, such as Strombidium , are non-constitutive mixotrophs that retain the plastid of their consumed prey ( Stoecker et al, 2009 ; Faure et al, 2019 ).…”