Microbial Community Structure-Function Relationships in Yaquina Bay Estuary Reveal Spatially Distinct Carbon and Nitrogen Cycling Capacities.

Brandon Kieft,Zhou Li,Xavier Mayali,Ryan S Mueller,Chongle Pan,Samuel Bryson,Robert Hettich,Byron C Crump

doi:10.3389/fmicb.2018.01282

Abstract

Linking microbial community structure to ecological processes requires understanding of the functional roles among individual populations and the factors that influence their distributions. These structure–function relationships are particularly difficult to disentangle in estuaries, due to highly variable physico-chemical conditions. Yet, examining microbe-mediated turnover of resources in these “bioreactor” ecosystems is critical for understanding estuarine ecology. In this study, a combined metagenomics and metaproteomics approach was used to show that the unequal distribution of microbial populations across the Yaquina Bay estuary led to a habitat-specific taxonomic and functional structure and a clear spatial distribution in microbe-mediated capacities for cycling of carbon and nitrogen. For example, size-fractionation revealed that communities inhabiting suspended particulate material encoded more diverse types of metabolisms (e.g., fermentation and denitrification) than those with a planktonic lifestyle, suggesting that the metabolic reactions can differ between size fractions of the same parcel of an estuarine water column. Similarly, communities inhabiting oligotrophic conditions in the lower estuary were enriched in genes involved in central carbon metabolism (e.g., TCA cycle), while communities in the upper estuary were enriched in genes typical of copiotrophic populations (e.g., cell growth, cell division). Integrating gene and protein data revealed that abundant populations of Flavobacteriales and Rhodobacterales encoded similar genomic functions, yet differed significantly in protein expression, dedicating a large proportion of their respective proteomes to rapid growth and division versus metabolic versatility and resource acquisition. This suggested potentially distinct life-strategies between these two co-occurring lineages and was concomitant with differing patterns of positive evolutionary selection on their encoded genes. Microbial communities and their functions across Yaquina Bay appear to be structured by population-level habitat preferences, resulting in spatially distinct elemental cycling, while within each community, forces such as competitive exclusion and evolutionary selection influence species life-strategies and may help maintain microbial diversity.

Highlights

Estuaries host communities of microorganisms that influence the exchange of nutrients between terrestrial, freshwater, and marine biomes (Cole and Caraco, 2001; Bauer et al, 2013)
Samples were taken from the top 1 m of the water column at a tidal height of ∼1.8 m near slack current (−0.1 m/s) in both the riverine end-member of the estuary and the coastal estuary mouth, which are separated by 8 km (Supplementary Figure S1)
The OTU-level Unifrac distance matrix and Order-level Euclidean distance matrix calculated from OTU counts yielded highly similar community beta-diversity patterns (Mantel’s test, Pearson r = 0.962, p < 0.001), and principal component analyses (PCA) likewise resulted in similar data shape between these two metrics (Procrustes symmetric correlation = 0.982, p < 0.001)

Summary

Introduction

Estuaries host communities of microorganisms that influence the exchange of nutrients between terrestrial, freshwater, and marine biomes (Cole and Caraco, 2001; Bauer et al, 2013). Biotic and abiotic dynamism is evident in estuaries during winter along the Oregon coast when heavy overland precipitation and steep nearshore topography cause coastal river flooding events that transport significant amounts of suspended particulate matter into estuarine water columns (Hickey and Banas, 2003; Hastings et al, 2012; Goñi et al, 2013) Microbes colonizing such particles represent an important component of aquatic biogeochemical cycles by acting to liberate particulate carbon and nutrients to the planktonic microbial loop through decomposition processes, and by supplementing higher trophic levels of the food web through resulting biomass production (Goulder, 1977; Wainright, 1990; Brown and Ozretich, 2009; Stocker, 2012). The functional roles of microbial communities and their relative influence on ecological processes occurring in different habitats within heterogeneous estuarine systems have seldom been examined (Simon et al, 2014)

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Results

Conclusion