Expression patterns reveal niche diversification in a marine microbial assemblage

Abstract

Resolving the ecological niches of coexisting marine microbial taxa is challenging due to the high species richness of microbial communities and the apparent functional redundancy in bacterial genomes and metagenomes. Here, we generated over 11 million Illumina reads of protein-encoding transcripts collected from well-mixed southeastern US coastal waters to characterize gene expression patterns distinguishing the ecological roles of hundreds of microbial taxa sharing the same environment. The taxa with highest in situ growth rates (based on relative abundance of ribosomal protein transcripts) were typically not the greatest contributors to community transcription, suggesting strong top-down ecological control, and their diverse transcriptomes indicated roles as metabolic generalists. The taxa with low in situ growth rates typically had low diversity transcriptomes dominated by specialized metabolisms. By identifying protein-encoding genes with atypically high expression for their level of conservation, unique functional roles of community members emerged related to substrate use (such as complex carbohydrates, fatty acids, methanesulfonate, taurine, tartrate, ectoine), alternative energy-conservation strategies (proteorhodopsin, AAnP, V-type pyrophosphatases, sulfur oxidation, hydrogen oxidation) and mechanisms for negotiating a heterogeneous environment (flagellar motility, gliding motility, adhesion strategies). On average, the heterotrophic bacterioplankton dedicated 7% of their transcriptomes to obtaining energy by non-heterotrophic means. This deep sequencing of a coastal bacterioplankton transcriptome provides the most highly resolved view of bacterioplankton niche dimensions yet available, uncovering a spectrum of unrecognized ecological strategies.

Deciphering associations between dissolved organic molecules and bacterial communities in a pelagic marine system

“…With regard to the active microbial community (RNA-based), the trends were less clear: representatives negatively correlating with the first canonical DOM axis included Alphaproteobacteria (seven OTUs) and Flavobacteria (three OTUs) and Gammaproteobacteria (three OTUs; Figure 6d); other Alphaproteobacteria (seven OTUs), Flavobacteria (three OTUs) and Deltaproteobacteria (two OTUs) correlated positively. These results, showing that bacteria of the same class can have opposing correlations to the DOM community, emphasize the possible niche partitioning below class level facilitated by the vast DOM molecular space (Hutchinson, 1961;Gifford et al, 2013).…”

“…Closely related and functionally similar taxa are found across similar habitats more often than expected by chance (Kraft et al, 2007;Teeling et al, 2012) and substratespecific allocation to the vast niche space offered by complex DOM may contribute to maintaining the highly diverse microbial communities in the oceans (Hutchinson, 1961;Zinger et al, 2011;Gifford et al, 2013).…”

Trimethylamine and trimethylamine N-oxide are supplementary energy sources for a marine heterotrophic bacterium: implications for marine carbon and nitrogen cycling

“…Cells with higher intracellular concentrations of ATP can respond faster to fluxes of organic matter associated with phytoplankton through ATP-mediated transport . Both SAR11 and Roseobacter cells devote a large amount of resources into the production of ABCtransporter systems to help facilitate the rapid uptake of essential nutrients (Sowell et al, 2008;2011;Williams et al, 2012;Gifford et al, 2013). Therefore, bacteria of the MRC and SAR11 clades capable of generating ATP from the catabolism of TMA and TMAO may have an ecological advantage through the efficient scavenging of nutrients in the surface waters.…”

“…Interestingly, in bacteria from the SAR11 clade, N limitation does not induce any of the genes involved in the catabolism of MAs, while energy starvation (in the dark) does induce some Smith et al, 2013). Moreover, an ammonium transporter (SAR_1310) located adjacent to the genes involved in MA catabolism is only induced under nitrogen-replete conditions and it has been proposed that this transporter is involved in ammonia export (Smith et al, 2013 the putative ammonium exporter related to both SAR11 and MRC clades are highly expressed in surface waters of the coast of Georgia (Gifford et al, 2013). At this site, genes involved in the catabolism of TMAO are also highly expressed in bacteria related to the SAR11 and MRC clades (Gifford et al, 2013).…”

Sizing up metatranscriptomics

“…For example, bacterial mRNA pools have provided assays of the bioreactive components of dissolved organic carbon pools based on transcriptome changes in amended seawater (McCarren et al, 2010;Poretsky et al, 2010;Shi et al, 2012); identified bacterial degradation pathways based on shifts in mRNA composition with increased substrate concentrations (Vila-Costa et al, 2010); characterized short-term reactions to altered CO 2 (Gilbert et al, 2008) and pollutant concentrations (de Menezes et al, 2012); and revealed niche differentiation among co-occurring autotrophs (Liu et al, 2012) and heterotrophs (Gifford et al, 2012). Changes in transcript inventories provide a sensitive window into the fluctuating cues perceived by microbes in their environment, and therefore the signals that drive changes in ecosystem function.…”