Metatranscriptome analyses indicate resource partitioning between diatoms in the field

Abstract

Diverse communities of marine phytoplankton carry out half of global primary production. The vast diversity of the phytoplankton has long perplexed ecologists because these organisms coexist in an isotropic environment while competing for the same basic resources (e.g., inorganic nutrients). Differential niche partitioning of resources is one hypothesis to explain this "paradox of the plankton," but it is difficult to quantify and track variation in phytoplankton metabolism in situ. Here, we use quantitative metatranscriptome analyses to examine pathways of nitrogen (N) and phosphorus (P) metabolism in diatoms that cooccur regularly in an estuary on the east coast of the United States (Narragansett Bay). Expression of known N and P metabolic pathways varied between diatoms, indicating apparent differences in resource utilization capacity that may prevent direct competition. Nutrient amendment incubations skewed N/P ratios, elucidating nutrient-responsive patterns of expression and facilitating a quantitative comparison between diatoms. The resource-responsive (RR) gene sets deviated in composition from the metabolic profile of the organism, being enriched in genes associated with N and P metabolism. Expression of the RR gene set varied over time and differed significantly between diatoms, resulting in opposite transcriptional responses to the same environment. Apparent differences in metabolic capacity and the expression of that capacity in the environment suggest that diatom-specific resource partitioning was occurring in Narragansett Bay. This high-resolution approach highlights the molecular underpinnings of diatom resource utilization and how cooccurring diatoms adjust their cellular physiology to partition their niche space.phytoplankton | diatom | nutrient physiology | niche partitioning | metatranscriptomics T he stability and primary productivity of ecosystems have long been linked to the diversity of primary producers (1, 2). This linkage is well documented in terrestrial systems (3-7) and is increasingly being established for marine systems (8-11). Marine phytoplankton generate roughly half of global primary production (12-14) and play a critical role in oceanic ecosystem structure and function. Within the phytoplankton, the diatoms generate an estimated 40% of primary production (15). Thus, diatoms alone exert a profound influence over marine primary production and global carbon (C) cycling, particularly in coastal margins and estuaries.Phytoplankton are extremely diverse, with estimates of over 200,000 extant species (16,17). This dramatic level of taxonomic diversity in the plankton is difficult to resolve with the apparently limited number of niches in the pelagic habitat because these organisms compete for the same two basic resources: light and nutrients. As was highlighted by Hutchinson (18), the phytoplankton violate Gause's law of competitive exclusion, which posits that two organisms competing for the same resources cannot coexist. Much thought has gone toward identifying the cause of the "pa...

Functional group-specific traits drive phytoplankton dynamics in the oligotrophic ocean

“…Within a functional group, the QMF was stable across time ( Fig. 2A), in contrast to the variability observed in coastal systems over similar time scales (17,18). This stability likely reflects the unique physiological attributes of oligotrophic phytoplankton as well as the comparatively static geochemical environment.…”

“…Between 18.1% and 20.7% of reads mapped to the MMETSP database were annotated with Kyoto Encyclopedia of Genes and Genomes (KEGG) orthology, elucidating differences in the mRNA distribution between functional groups at the pathway level. Looking at the module level, the general distribution of transcripts in proportion to the total was assessed using quantitative metabolic fingerprint(ing) (QMF) (17). Diatoms have a larger proportion of mRNA in the transport-related system (e.g., metallic cation, vitamin B 12 , phosphate, amino acid) compared with haptophytes and dinoflagellates ( Fig.…”

“…Molecular-level tools that can track transcripts, proteins, or even metabolites and biochemicals in a taxon-specific way are increasingly being used in cultures and field populations to track metabolic capacity and physiological responses (16)(17)(18)(19)(20)(21)(22)(23). Molecular assessment of physiology for eukaryotic populations is most tractable in coastal systems with high biomass (17,18); thus, in oligotrophic ocean regions, molecular studies of physiology have typically been limited to the numerically abundant members of the microbial community: picoplankton (cyanobacteria, heterotrophic bacteria, and small picoeukaryotes).…”

“…Molecular assessment of physiology for eukaryotic populations is most tractable in coastal systems with high biomass (17,18); thus, in oligotrophic ocean regions, molecular studies of physiology have typically been limited to the numerically abundant members of the microbial community: picoplankton (cyanobacteria, heterotrophic bacteria, and small picoeukaryotes). Groundbreaking studies have demonstrated the responsiveness of the dominant picoplankton community to pulses of deep seawater (DSW) (24) and dissolved organic matter (DOM) (25), as well as the diel synchrony of the photosynthetic and heterotrophic communities (20), yet were limited in their coverage of the rare, large eukaryotic fraction due to both the low biomass of their standing stock and the lack of reference sequences.…”

Molecular insights into a dinoflagellate bloom

“…Sequencing of mRNA transcripts from the environment and subsequent analysis of gene expression patterns (commonly referred to as metatranscriptomics) has been shown to be a powerful tool for identifying the distinct cellular-level processes conducted by bloom-forming taxa within the background of all metabolic activities performed within a mixed plankton assemblage (Cooper et al, 2014). Recent applications of metatranscriptomic approaches have provided new insights into microalgal processes in natural marine environments and include characterization of the phytoplankton response to iron enrichment (Marchetti et al, 2012) and resource partitioning among distinct phytoplankton species in nutrient-rich coastal environments (Alexander et al, 2015).…”