PhD student, University of Cambridge
Linking terrestrial and aquatic ecosystems: how lake sediment microbes decompose terrestrial carbon
The boreal ecozone holds an estimated 60% of the world’s freshwater, but lakes in this region tend to be nutrient-poor and less productive, making their production reliant on carbon subsidies from riparian litterfall. The availability of these carbon subsidies for aquatic food webs, however, depends on microbial communities in lake sediment. Little is known about how the taxonomic and functional diversity of heterotrophic bacteria might influence the rate at which this terrestrial organic matter (OM) is decomposed. Drawing upon biodiversity-ecosystem functioning theory, we predicted that decomposition rates, indicative of both food web production and biogeochemical cycling, increase with the taxonomic and functional diversity of bacterial communities that add new abilities to degrade OM. We characterized both bacterial community composition and microbial functional traits in nearshore sediments from 8 catchments along a gradient of terrestrial OM inputs using next-generation sequencing (16S rRNA amplicon sequencing and shotgun metagenomics). We found that both OM quantity and taxonomic diversity, and not functional diversity, promoted OM decomposition rates. The effect of taxonomic diversity on OM decomposition was mostly attributable to differences in bacterial communities among catchments irrespective of their environmental conditions, suggesting that colonization history rather than habitat-based filtering influenced community assembly. Monthly sampling of the microbial communities present in experimental mesocoms was done in parallel in order to understand the mechanisms of this colonization process. Preliminary analyses revealed the importance of founder taxa in determining community structure, and consequently ecosystem functioning. This study highlights the role of microbial communities in facilitating the transfer of resources from terrestrial ecosystems, and improves our understanding of how catchment disturbances may affect boreal aquatic ecosystems.
Abstract: Microbes are dominant drivers of biogeochemical processes, yet drawing a global picture of functional diversity, microbial community structure, and their ecological determinants remains a grand challenge. We analyzed 7.2 terabases of metagenomic data from 243 Tara Oceans samples from 68 locations in epipelagic and mesopelagic waters across the globe to generate an ocean microbial reference gene catalog with >40 million nonredundant, mostly novel sequences from viruses, prokaryotes, and picoeukaryotes. Using 139 prokaryote-enriched samples, containing >35,000 species, we show vertical stratification with epipelagic community composition mostly driven by temperature rather than other environmental factors or geography. We identify ocean microbial core functionality and reveal that >73% of its abundance is shared with the human gut microbiome despite the physicochemical differences between these two ecosystems.
Pub.: 23 May '15, Pinned: 29 Jun '17
Abstract: Local diversity (within-sample or alpha diversity) is often implicated as a cause of success or failure of a microbial community. However, the relationships between diversity and emergent properties of a community, such as its stability, productivity or invasibility, are much more nuanced. I argue that diversity without context provides limited insights into the mechanisms underpinning community patterns. I provide examples from traditional and microbial ecology to discuss common complications and assumptions about within-sample diversity that may prevent us from digging deeper into the more specific mechanisms underpinning community outcomes. I suggest that measurement of diversity should serve as a starting point for further inquiry of ecological mechanisms rather than an 'answer' to community outcomes.The ISME Journal advance online publication, 16 September 2016; doi:10.1038/ismej.2016.118.
Pub.: 17 Sep '16, Pinned: 29 Jun '17
Abstract: Ecologists have long studied the temporal dynamics of plant and animal communities with much less attention paid to the temporal dynamics exhibited by microbial communities. As a result, we do not know if overarching temporal trends exist for microbial communities or if changes in microbial communities are generally predictable with time. Using microbial time series assessed via high-throughput sequencing, we conducted a meta-analysis of temporal dynamics in microbial communities, including 76 sites representing air, aquatic, soil, brewery wastewater treatment, human- and plant-associated microbial biomes. We found that temporal variability in both within- and between-community diversity was consistent among microbial communities from similar environments. Community structure changed systematically with time in less than half of the cases, and the highest rates of change were observed within ranges of 1 day to 1 month for all communities examined. Microbial communities exhibited species-time relationships (STRs), which describe the accumulation of new taxa to a community, similar to those observed previously for plant and animal communities, suggesting that STRs are remarkably consistent across a broad range of taxa. These results highlight that a continued integration of microbial ecology into the broader field of ecology will provide new insight into the temporal patterns of microbial and 'macro'-bial communities alike.
Pub.: 12 Apr '13, Pinned: 29 Jun '17
Abstract: Despite the importance of microbial communities for ecosystem services and human welfare, the relationship between microbial diversity and multiple ecosystem functions and services (that is, multifunctionality) at the global scale has yet to be evaluated. Here we use two independent, large-scale databases with contrasting geographic coverage (from 78 global drylands and from 179 locations across Scotland, respectively), and report that soil microbial diversity positively relates to multifunctionality in terrestrial ecosystems. The direct positive effects of microbial diversity were maintained even when accounting simultaneously for multiple multifunctionality drivers (climate, soil abiotic factors and spatial predictors). Our findings provide empirical evidence that any loss in microbial diversity will likely reduce multifunctionality, negatively impacting the provision of services such as climate regulation, soil fertility and food and fibre production by terrestrial ecosystems.
Pub.: 28 Jan '16, Pinned: 29 Jun '17
Abstract: Lake consumers are supported by autochthonous organic matter produced by photosynthesis within the aquatic ecosystem and imported allochthonous material produced outside the ecosystem. To evaluate carbon sources that support fish growth, we enriched a 26 ha lake with inorganic 13C. This labeled the autochthonous primary production and allowed us to determine the extent to which invertebrates in fish diets were supported by this autochthonous carbon. Fish autochthony was defined as the proportion ranging from 0 to 1 of fish growth derived from aquatic primary production. This proportion was calculated using the weighted average of each diet taxa’s contribution to fish growth along with the autochthony of diet taxa estimated with dynamic models of δ13C time series. Age 0 bluegill (Lepomis macrochirus) and yellow perch (Perca flavescens) had the highest autochthony (0.56, 0.57, respectively) because of greater use of zooplankton that were highly dependent on phytoplankton. Older fishes (age 1 and above) of all species had similar estimates of autochthony (mean=0.47 standard deviation=0.04) derived from feeding on either benthic invertebrates or other fishes. Proportional contribution of terrestrial prey (primarily terrestrial beetles) to fish growth was highest for bluegill (0.07–0.22) and substantially lower (<0.04) for largemouth bass (Micropterus salmoides) and yellow perch. Across species and ages ~ 45% of fish growth could not be attributed to terrestrial prey items or current autochthonous primary production. This residual detrital carbon source is a mixture of allochthonous material and autochthonous material derived from primary production prior to the 13C addition. Fish growth and production in the study lake were not tightly coupled to the current season’s primary production. Nearly half of the organic carbon supporting fish growth came from prior autochthonous primary production or allochthonous sources.
Pub.: 22 Sep '08, Pinned: 29 Jun '17
Abstract: Seed banks are believed to contribute to compositional changes within and across microbial assemblages, but the application of this concept to natural communities remains challenging. Here we describe the core seed bank of a bacterial metacommunity from a boreal watershed, using the spatial distribution of bacterial operational taxonomic units (OTUs) across 223 heterogeneous terrestrial, aquatic and phyllosphere bacterial assemblages. Taxa were considered potential seeds if they transitioned from rare to abundant somewhere within the metacommunity and if they were ubiquitous and able to persist under unfavorable conditions, the latter assessed by checking their presence in three deeply sequenced samples (one soil, one river and one lake, 2.2-3 million reads per sample). We show that only a small fraction (13%) of all detected OTUs constitute a metacommunity seed bank that is shared between all terrestrial and aquatic communities, but not by phyllosphere assemblages, which seem to recruit from a different taxa pool. Our results suggest directional recruitment driven by the flow of water in the landscape, since most aquatic sequences were associated to OTUs found in a single deeply-sequenced soil sample, but only 45% of terrestrial sequences belonged to OTUs found in the two deeply-sequenced aquatic communities. Finally, we hypothesize that extreme rarity, and its interplay with water residence time and growth rates, may further constrain the size of the potential seed bank.The ISME Journal advance online publication, 6 June 2017; doi:10.1038/ismej.2017.67.
Pub.: 07 Jun '17, Pinned: 29 Jun '17
Abstract: Bacteria inhabiting boreal freshwaters are part of metacommunities where local assemblages are often linked by the flow of water in the landscape, yet the resulting spatial structure and the boundaries of the network metacommunity have never been explored. Here, we reconstruct the spatial structure of the bacterial metacommunity in a complex boreal aquatic network by determining the taxonomic composition of bacterial communities along the entire terrestrial/aquatic continuum, including soil and soilwaters, headwater streams, large rivers and lakes. We show that the network metacommunity has a directional spatial structure driven by a common terrestrial origin of aquatic communities, which are numerically dominated by taxa recruited from soils. Local community assembly is driven by variations along the hydrological continuum in the balance between mass effects and species sorting of terrestrial taxa, and seems further influenced by priority effects related to the spatial sequence of entry of soil bacteria into the network.
Pub.: 27 Aug '15, Pinned: 27 Jun '17
Abstract: We review the biogeography of microorganisms in light of the biogeography of macroorganisms. A large body of research supports the idea that free-living microbial taxa exhibit biogeographic patterns. Current evidence confirms that, as proposed by the Baas-Becking hypothesis, 'the environment selects' and is, in part, responsible for spatial variation in microbial diversity. However, recent studies also dispute the idea that 'everything is everywhere'. We also consider how the processes that generate and maintain biogeographic patterns in macroorganisms could operate in the microbial world.
Pub.: 18 Jan '06, Pinned: 27 Jun '17
Abstract: Aquatic ecosystems are fuelled by biogeochemical inputs from surrounding lands and within-lake primary production. Disturbances that change these inputs may affect how aquatic ecosystems function and deliver services vital to humans. Here we test, using a forest cover gradient across eight separate catchments, whether disturbances that remove terrestrial biomass lower organic matter inputs into freshwater lakes, thereby reducing food web productivity. We focus on deltas formed at the stream-lake interface where terrestrial-derived particulate material is deposited. We find that organic matter export increases from more forested catchments, enhancing bacterial biomass. This transfers energy upwards through communities of heavier zooplankton, leading to a fourfold increase in weights of planktivorous young-of-the-year fish. At least 34% of fish biomass is supported by terrestrial primary production, increasing to 66% with greater forest cover. Habitat tracers confirm fish were closely associated with individual catchments, demonstrating that watershed protection and restoration increase biomass in critical life-stages of fish.
Pub.: 12 Jun '14, Pinned: 27 Jun '17
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