Diversity begets diversity: chemical and microbial diversity co-vary in freshwater to influence ecosystem functioning

Invisible to the naked eye lies a tremendous diversity of organic molecules and organisms that make major contributions to important biogeochemical cycles. However, how the diversity and composition of these two communities are inter-linked remains poorly characterised in freshwaters, despite the potential for chemical and microbial diversity to promote one another. Here we exploited gradients in chemodiversity within a common microbial pool to test how chemical and biological diversity covary and characterized the implications for ecosystem functioning. We found that both chemodiversity and genes associated with organic matter decomposition increased as more plant litterfall accumulated in experimental lake sediments, consistent with scenarios of future environmental change. Chemical and microbial diversity were also positively correlated, with dissolved organic matter having stronger effects on microbes than vice versa. Under our experimental scenarios that increased sediment organic matter from 5 to 25% or darkened overlying waters by 2.5-times, the resulting increases in chemodiversity could increase greenhouse gas concentrations in lake sediments by an average of 1.5- to 2.7-times, when all the other effects of litterfall and water color were considered. Our results open a major new avenue for research in aquatic ecosystems by exposing connections between chemical and microbial diversity and their implications for the global carbon cycle in greater detail than ever before.Funding came from a Natural Environment Research Council grant NE/L006561/1 to AJT and a Gates Cambridge Scholarship to AF

Forest defoliator outbreaks alter nutrient cycling in northern waters.

Insect defoliators alter biogeochemical cycles from land into receiving waters by consuming terrestrial biomass and releasing biolabile frass. Here, we related insect outbreaks to water chemistry across 12 boreal lake catchments over 32-years. We report, on average, 27% lower dissolved organic carbon (DOC) and 112% higher dissolved inorganic nitrogen (DIN) concentrations in lake waters when defoliators covered entire catchments and reduced leaf area. DOC reductions reached 32% when deciduous stands dominated. Within-year changes in DOC from insect outbreaks exceeded 86% of between-year trends across a larger dataset of 266 boreal and north temperate lakes from 1990 to 2016. Similarly, within-year increases in DIN from insect outbreaks exceeded local, between-year changes in DIN by 12-times, on average. As insect defoliator outbreaks occur at least every 5 years across a wider 439,661 km2 boreal ecozone of Ontario, we suggest they are an underappreciated driver of biogeochemical cycles in forest catchments of this region.Natural Environment Research Council (NE/L006561/1) Ontario Centres of Excellence (OCE/27649) Natural Sciences and Engineering Research Council of Canada (NSERC/509182-17

Feasting on terrestrial organic matter: Dining in a dark lake changes microbial decomposition.

Boreal lakes are major components of the global carbon cycle, partly because of sediment-bound heterotrophic microorganisms that decompose within-lake and terrestrially derived organic matter (t-OM). The ability for sediment bacteria to break down and alter t-OM may depend on environmental characteristics and community composition. However, the connection between these two potential drivers of decomposition is poorly understood. We tested how bacterial activity changed along experimental gradients in the quality and quantity of t-OM inputs into littoral sediments of two small boreal lakes, a dark and a clear lake, and measured the abundance of operational taxonomic units and functional genes to identify mechanisms underlying bacterial responses. We found that bacterial production (BP) decreased across lakes with aromatic dissolved organic matter (DOM) in sediment pore water, but the process underlying this pattern differed between lakes. Bacteria in the dark lake invested in the energetically costly production of extracellular enzymes as aromatic DOM increased in availability in the sediments. By contrast, bacteria in the clear lake may have lacked the nutrients and/or genetic potential to degrade aromatic DOM and instead mineralized photo-degraded OM into CO2 . The two lakes differed in community composition, with concentrations of dissolved organic carbon and pH differentiating microbial assemblages. Furthermore, functional genes relating to t-OM degradation were relatively higher in the dark lake. Our results suggest that future changes in t-OM inputs to lake sediments will have different effects on carbon cycling depending on the potential for photo-degradation of OM and composition of resident bacterial communities

Universal microbial reworking of dissolved organic matter along soil gradients

Soils are losing increasing amounts of carbon annually to freshwaters as dissolved organic matter (DOM), which, if degraded, can offset their carbon sink capacity. However, the processes underlying DOM degradation across environments are poorly understood. Here we show DOM changes similarly along soil-aquatic gradients irrespective of environmental differences. Using ultrahigh-resolution mass spectrometry, we track DOM along soil depths and hillslope positions in forest catchments and relate its composition to soil microbiomes and physico-chemical conditions. Along depths and hillslopes, we find carbohydrate-like and unsaturated hydrocarbon-like compounds increase in abundance-weighted mass, and the expression of genes essential for degrading plant-derived carbohydrates explains >50% of the variation in abundance of these compounds. These results suggest that microbes transform plant-derived compounds, leaving DOM to become increasingly dominated by the same (i.e., universal), difficult-to-degrade compounds as degradation proceeds. By synthesising data from the land-to-ocean continuum, we suggest these processes generalise across ecosystems and spatiotemporal scales. Such general degradation patterns can help predict DOM composition and reactivity along environmental gradients to inform management of soil-to-stream carbon losses

Universal microbial reworking of dissolved organic matter along environmental gradients

Acknowledgements: We are thankful to K Waxenberg, W Pallier, and L Mahony (Cambridge) for help with fieldwork. Additional support was provided by K. Klapproth and I Ulber with FT-ICR-MS measurements and C Schmalsch with LC-OCD samples. We also thank staff at the Natural Resources Canada – Canadian Forest Service (NRCan-CFS) for considerable support, including with logistics (K Webster, P Hazlett), development of extraction and assay protocols (V Rouleau, M-J Morency), conducting laboratory extractions and assays (E Smenderovac, D Chartrand, M-J Morency), and general field and laboratory assistance (J Schadenberg and many others). This work was funded by a Gates Cambridge Scholarship (OPP1144) awarded to E.C.F., NRCan-CFS Cumulative Effects programme awarded to E.J.S.E., H2020 ERC Grant FLUFLUX (716196) to G.S., H2020 ERC Grant sEEIngDOM (804673) to A.J.T., and grant from the Genomic Research and Development Initiative of the Government of Canada to C.M. and E.J.S.E.Funder: Genomic Research and Development Initiative of the Government of Canada, NRCan-CFS Cumulative Effects program awardsAbstractSoils are losing increasing amounts of carbon annually to freshwaters as dissolved organic matter (DOM), which, if degraded, can offset their carbon sink capacity. However, the processes underlying DOM degradation across environments are poorly understood. Here we show DOM changes similarly along soil-aquatic gradients irrespective of environmental differences. Using ultrahigh-resolution mass spectrometry, we track DOM along soil depths and hillslope positions in forest catchments and relate its composition to soil microbiomes and physico-chemical conditions. Along depths and hillslopes, we find carbohydrate-like and unsaturated hydrocarbon-like compounds increase in abundance-weighted mass, and the expression of genes essential for degrading plant-derived carbohydrates explains &gt;50% of the variation in abundance of these compounds. These results suggest that microbes transform plant-derived compounds, leaving DOM to become increasingly dominated by the same (i.e., universal), difficult-to-degrade compounds as degradation proceeds. By synthesising data from the land-to-ocean continuum, we suggest these processes generalise across ecosystems and spatiotemporal scales. Such general degradation patterns can help predict DOM composition and reactivity along environmental gradients to inform management of soil-to-stream carbon losses.</jats:p

Microbiome functioning depends on individual and interactive effects of the environment and community structure.

How ecosystem functioning changes with microbial communities remains an open question in natural ecosystems. Both present-day environmental conditions and historical events, such as past differences in dispersal, can have a greater influence over ecosystem function than the diversity or abundance of both taxa and genes. Here, we estimated how individual and interactive effects of microbial community structure defined by diversity and abundance, present-day environmental conditions, and an indicator of historical legacies influenced ecosystem functioning in lake sediments. We studied sediments because they have strong gradients in all three of these ecosystem properties and deliver important functions worldwide. By characterizing bacterial community composition and functional traits at eight sites fed by discrete and contrasting catchments, we found that taxonomic diversity and the normalized abundance of oxidase-encoding genes explained as much variation in CO2 production as present-day gradients of pH and organic matter quantity and quality. Functional gene diversity was not linked to CO2 production rates. Surprisingly, the effects of taxonomic diversity and normalized oxidase abundance in the model predicting CO2 production were attributable to site-level differences in bacterial communities unrelated to the present-day environment, suggesting that colonization history rather than habitat-based filtering indirectly influenced ecosystem functioning. Our findings add to limited evidence that biodiversity and gene abundance explain patterns of microbiome functioning in nature. Yet we highlight among the first time how these relationships depend directly on present-day environmental conditions and indirectly on historical legacies, and so need to be contextualized with these other ecosystem properties.Support for this work came from NERC Standard Grant NE/L006561/1 and Gatsby Fellowship GAT2962 to Andrew J. Tanentzap

Plant Litter Type Dictates Microbial Communities Responsible for Greenhouse Gas Production in Amended Lake Sediments.

The microbial communities of lake sediments play key roles in carbon cycling, linking lakes to their surrounding landscapes and to the global climate system as incubators of terrestrial organic matter and emitters of greenhouse gasses, respectively. Here, we amended lake sediments with three different plant leaf litters: a coniferous forest mix, deciduous forest mix, cattails (Typha latifolia) and then examined the bacterial, fungal and methanogen community profiles and abundances. Polyphenols were found to correlate with changes in the bacterial, methanogen, and fungal communities; most notably dominance of fungi over bacteria as polyphenol levels increased with higher abundance of the white rot fungi Phlebia spp. Additionally, we saw a shift in the dominant orders of fermentative bacteria with increasing polyphenol levels, and differences in the dominant methanogen groups, with high CH4 production being more strongly associated with generalist groups of methanogens found at lower polyphenol levels. Our present study provides insights into and basis for future study on how shifting upland and wetland plant communities may influence anaerobic microbial communities and processes in lake sediments, and may alter the fate of terrestrial carbon entering inland waters.Funding was provided by NERC Standard Grant NE/L006561/1 to AJT and 521 NSERC Discovery and Canada Research Chair funds to NB

Viruses direct carbon cycling in lake sediments under global change.

Global change is altering the vast amount of carbon cycled by microbes between land and freshwater, but how viruses mediate this process is poorly understood. Here, we show that viruses direct carbon cycling in lake sediments, and these impacts intensify with future changes in water clarity and terrestrial organic matter (tOM) inputs. Using experimental tOM gradients within sediments of a clear and a dark boreal lake, we identified 156 viral operational taxonomic units (vOTUs), of which 21% strongly increased with abundances of key bacteria and archaea, identified via metagenome-assembled genomes (MAGs). MAGs included the most abundant prokaryotes, which were themselves associated with dissolved organic matter (DOM) composition and greenhouse gas (GHG) concentrations. Increased abundances of virus-like particles were separately associated with reduced bacterial metabolism and with shifts in DOM toward amino sugars, likely released by cell lysis rather than higher molecular mass compounds accumulating from reduced tOM degradation. An additional 9.6% of vOTUs harbored auxiliary metabolic genes associated with DOM and GHGs. Taken together, these different effects on host dynamics and metabolism can explain why abundances of vOTUs rather than MAGs were better overall predictors of carbon cycling. Future increases in tOM quantity, but not quality, will change viral composition and function with consequences for DOM pools. Given their importance, viruses must now be explicitly considered in efforts to understand and predict the freshwater carbon cycle and its future under global environmental change