Abstract
Microorganisms aggregated into matrix-enclosed biofilms dominate microbial life in most natural, engineered, and medical systems. Despite this, the ecological adaptations and metabolic trade-offs of the formation of complex biofilms are currently poorly understood. Here, exploring the dynamics of bacterial ribosomal RNA operon (rrn) copy numbers, we unravel the genomic underpinning of the formation and success of stream biofilms that contain hundreds of bacterial taxa. Experimenting with stream biofilms, we found that nascent biofilms in eutrophic systems had reduced lag phases and higher growth rates, and more taxa with higher rrn copy number than biofilms from oligotrophic systems. Based on these growth-related traits, our findings suggest that biofilm succession was dominated by slow-but-efficient bacteria likely with leaky functions, such as the production of extracellular polymeric substances at the cost of rapid growth. Expanding our experimental findings to biofilms from 140 streams, we found that rrn copy number distribution reflects functional trait allocation and ecological strategies of biofilms to be able to thrive in fluctuating environments. These findings suggest that alternative trade-offs dominating over rate-yield trade-offs contribute to the evolutionary success of stream biofilms.
Highlights
After assignment of rrn copy numbers, we retained operational taxonomic units (OTUs, n = 9.676) belonging to 182 genera common to all samples (Supplementary Figure 1). We considered these genera as typical biofilm formers in streams
Published in partnership with Nanyang Technological University inefficient growth depending on rrn copy numbers,[11,19] we genera, respectively (Supplementary Figure 2)
Community average (±standard deviation) rrn copy numbers based on taxa presence was 3.16 ± 0.15 in biofilms grown under oligotrophic conditions and 3.05 ± 0.11 in biofilms grown under eutrophic conditions
Summary
Over the last 3.5 billion years, microbial biofilms have undergone multiple evolutionary cycles over which they have developed ecological strategies to exploit diverse niches on Earth.[1,2] In stream ecosystems, biofilms dominate microbial life, regulate critical ecosystem processes and biogeochemical fluxes that are even of global relevance.[3,4] The assembly of thousands of bacterial taxa into these complex biofilms and their biodiversity dynamics have been uncovered over the last years.[5,6,7,8] the genomic determinants that possibly underlie the formation of complex biofilms and their evolutionary success are not understood.The availability of cultivation-independent estimates of rrn copy numbers has recently reinvigorated interests in the genomic underpinning of metabolic trade-offs of diverse bacterial communities.[9,10,11] This is a major step forward to understand how community-aggregated functional traits give rise to ecological strategies driving adaptations to natural environments.[12,13,14] Genes encoding the 5S, 16S, and 23S ribosomal RNA are organized into an operon (rrn) on bacterial genomes. We analyzed the succession of rrn copy numbers in biofilms grown in stream microcosms and containing hundreds of bacterial taxa.[22] We hypothesized that the distribution of rrn copy numbers in natural biofilms reflects trade-offs between resource use efficiency and growth rate during biofilm formation.
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