Abstract
Phototrophic biofilms are ubiquitous in freshwater and marine environments where they are critical for biogeochemical cycling, food webs and in industrial applications. In streams, phototrophic biofilms dominate benthic microbial life and harbour an immense prokaryotic and eukaryotic microbial biodiversity with biotic interactions across domains and trophic levels. Here, we examine how community structure and function of these biofilms respond to varying light availability, as the crucial energy source for phototrophic biofilms. Using metatranscriptomics, we found that under light limitation‐dominant phototrophs, including diatoms and cyanobacteria, displayed a remarkable plasticity in their photosynthetic machinery manifested as higher abundance of messenger RNAs (mRNAs) involved in photosynthesis and chloroplast ribosomal RNA. Under higher light availability, bacterial mRNAs involved in phosphorus metabolism, mainly from Betaproteobacteria and Cyanobacteria, increased, likely compensating for nutrient depletion in thick biofilms with high biomass. Consumers, including diverse ciliates, displayed community shifts indicating preferential grazing on algae instead of bacteria under higher light. For the first time, we show that the functional integrity of stream biofilms under variable light availability is maintained by structure–function adaptations on several trophic levels. Our findings shed new light on complex biofilms, or “microbial jungles”, where in analogy to forests, diverse and multitrophic level communities lend stability to ecosystem functioning. This multitrophic level perspective, coupling metatranscriptomics to process measurements, could advance understanding of microbial‐driven ecosystems beyond biofilms, including planktonic and soil environments.
Highlights
Taxonomic and phylogenetic diversity in natural microbial communities is massive (Locey & Lennon, 2016; Torsvik, Goksøyr, & Daae, 1990)
We found that under light limitation-dominant phototrophs, including diatoms and cyanobacteria, displayed a remarkable plasticity in their photosynthetic machinery manifested as higher abundance of messenger RNAs involved in photosynthesis and chloroplast ribosomal RNA
Bacterial messenger RNAs (mRNAs) involved in phosphorus metabolism, mainly from Betaproteobacteria and Cyanobacteria, increased, likely compensating for nutrient depletion in thick biofilms with high biomass
Summary
Taxonomic and phylogenetic diversity in natural microbial communities is massive (Locey & Lennon, 2016; Torsvik, Goksøyr, & Daae, 1990). Despite the methodological leaps that have enabled description of this biodiversity, from deep sequencing of the prokaryotic rare biosphere (Sogin et al, 2006) to phylogenetic inference of novel prokaryotic and eukaryotic lineages (Hug et al, 2016; Jones et al, 2011), a tendency to address prokaryotes and eukaryotes separately has prevailed in most biodiversity studies This inhibits the understanding of the ecology of complex microbial communities that include organisms across all domains of life on several trophic levels. According to the light:nutrient hypothesis (Sterner, Elser, & Fee, 1997), alterations in these resources affect periphyton C:P ratios, with implications for higher trophic levels and ecosystem function (Fanta, Hill, Smith, & Roberts, 2010; Hill, Rinchard, & Czesny, 2011) As predicted by this hypothesis, increased production and exudation of C-rich photosynthates by phototrophs under high light, P-depleted conditions, fuel bacterial heterotrophic metabolism. Biofilm consumers such as microbial grazers will experience a shift in their food source as light availability alters the community composition within the phototroph and heterotrophic bacteria functional groups, causing a secondary shift in the community composition of consumers
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