Jay Lennon | Indiana University (original) (raw)

Papers by Jay Lennon

Frontiers in microbiology, 2015

Dormancy is a life history trait that may have important implications for linking microbial commu... more Dormancy is a life history trait that may have important implications for linking microbial communities to the functioning of natural and managed ecosystems. Rapid changes in environmental cues may resuscitate dormant bacteria and create pulses of ecosystem activity. In this study, we used heavy-water (H(18) 2O) stable isotope probing (SIP) to identify fast-growing bacteria that were associated with pulses of trace gasses (CO2, CH4, and N2O) from different ecosystems [agricultural site, grassland, deciduous forest, and coniferous forest (CF)] following a soil-rewetting event. Irrespective of ecosystem type, a large fraction (69-74%) of the bacteria that responded to rewetting were below detection limits in the dry soils. Based on the recovery of sequences, in just a few days, hundreds of rare taxa increased in abundance and in some cases became dominant members of the rewetted communities, especially bacteria belonging to the Sphingomonadaceae, Comamonadaceae, and Oxalobacteraceae. ...

Frontiers in Microbiology, 2014

In ecology, biodiversity-ecosystem functioning (BEF) research has seen a shift in perspective fro... more In ecology, biodiversity-ecosystem functioning (BEF) research has seen a shift in perspective from taxonomy to function in the last two decades, with successful application of trait-based approaches. This shift offers opportunities for a deeper mechanistic understanding of the role of biodiversity in maintaining multiple ecosystem processes and services. In this paper, we highlight studies that have focused on BEF of microbial communities with an emphasis on integrating trait-based approaches to microbial ecology. In doing so, we explore some of the inherent challenges and opportunities of understanding BEF using microbial systems. For example, microbial biologists characterize communities using gene phylogenies that are often unable to resolve functional traits. Additionally, experimental designs of existing microbial BEF studies are often inadequate to unravel BEF relationships. We argue that combining eco-physiological studies with contemporary molecular tools in a trait-based framework can reinforce our ability to link microbial diversity to ecosystem processes. We conclude that such trait-based approaches are a promising framework to increase the understanding of microbial BEF relationships and thus generating systematic principles in microbial ecology and more generally ecology.

The ISME journal, Jan 23, 2014

For any enzyme-catalyzed reaction to occur, the corresponding protein-encoding genes and transcri... more For any enzyme-catalyzed reaction to occur, the corresponding protein-encoding genes and transcripts are necessary prerequisites. Thus, a positive relationship between the abundance of gene or transcripts and corresponding process rates is often assumed. To test this assumption, we conducted a meta-analysis of the relationships between gene and/or transcript abundances and corresponding process rates. We identified 415 studies that quantified the abundance of genes or transcripts for enzymes involved in carbon or nitrogen cycling. However, in only 59 of these manuscripts did the authors report both gene or transcript abundance and rates of the appropriate process. We found that within studies there was a significant but weak positive relationship between gene abundance and the corresponding process. Correlations were not strengthened by accounting for habitat type, differences among genes or reaction products versus reactants, suggesting that other ecological and methodological fact...

The ISME Journal, 2013

Although numerous studies have investigated changes in soil microbial communities across space, q... more Although numerous studies have investigated changes in soil microbial communities across space, questions about the temporal variability in these communities and how this variability compares across soils have received far less attention. We collected soils on a monthly basis (May to November) from replicated plots representing three land-use types (conventional and reduced-input row crop agricultural plots and early successional grasslands) maintained at a research site in Michigan, USA. Using barcoded pyrosequencing of the 16S rRNA gene, we found that the agricultural and early successional land uses harbored unique soil bacterial communities that exhibited distinct temporal patterns. a-Diversity, the numbers of taxa or lineages, was significantly influenced by the sampling month with the temporal variability in a-diversity exceeding the variability between land-use types. In contrast, differences in community composition across landuse types were reasonably constant across the 7-month period, suggesting that the time of sampling is less important when assessing b-diversity patterns. Communities in the agricultural soils were most variable over time and the changes were significantly correlated with soil moisture and temperature. Temporal shifts in bacterial community composition within the successional grassland plots were less predictable and are likely a product of complex interactions between the soil environment and the more diverse plant community. Temporal variability needs to be carefully assessed when comparing microbial diversity across soil types and the temporal patterns in microbial community structure can not necessarily be generalized across land uses, even if those soils are exposed to the same climatic conditions.

PLoS ONE, 2013

There is growing evidence that terrestrial ecosystems are exporting more dissolved organic carbon... more There is growing evidence that terrestrial ecosystems are exporting more dissolved organic carbon (DOC) to aquatic ecosystems than they did just a few decades ago. This ''browning'' phenomenon will alter the chemistry, physics, and biology of inland water bodies in complex and difficult-to-predict ways. Experiments provide an opportunity to elucidate how browning will affect the stability and functioning of aquatic ecosystems. However, it is challenging to obtain sources of DOC that can be used for manipulations at ecologically relevant scales. In this study, we evaluated a commercially available source of humic substances (''Super Hume'') as an analog for natural sources of terrestrial DOC. Based on chemical characterizations, comparative surveys, and whole-ecosystem manipulations, we found that the physical and chemical properties of Super Hume are similar to those of natural DOC in aquatic and terrestrial ecosystems. For example, Super Hume attenuated solar radiation in ways that will not only influence the physiology of aquatic taxa but also the metabolism of entire ecosystems. Based on its chemical properties (high lignin content, high quinone content, and low C:N and C:P ratios), Super Hume is a fairly recalcitrant, low-quality resource for aquatic consumers. Nevertheless, we demonstrate that Super Hume can subsidize aquatic food webs through 1) the uptake of dissolved organic constituents by microorganisms, and 2) the consumption of particulate fractions by larger organisms (i.e., Daphnia). After discussing some of the caveats of Super Hume, we conclude that commercial sources of humic substances can be used to help address pressing ecological questions concerning the increased export of terrestrial DOC to aquatic ecosystems.

A recent analysis revealed that most environmental microbiologists neglect replication in their s... more A recent analysis revealed that most environmental microbiologists neglect replication in their science (Prosser, 2010). Of all peer-reviewed papers published during 2009 in the field's leading journals, slightly more than 70% lacked replication when it came to analyzing microbial community data. The paucity of replication is viewed as an 'endemic' and 'embarrassing' problem that amounts to 'bad science', or worse yet, as the title suggests, lying (Prosser, 2010). Although replication is an important component of experimental design, it is possible to do good science without replication. There are various quantitative techniques -some old, some new -that, when used properly, will allow environmental microbiologists to make strong statistical conclusions from experimental and comparative data. Here, I provide examples where unreplicated data can be used to test hypotheses and yield novel information in a statistically robust manner.

Subsidies are donor-controlled inputs of nutrients and energy that can affect ecosystem-level pro... more Subsidies are donor-controlled inputs of nutrients and energy that can affect ecosystem-level processes in a recipient environment. Lake ecosystems receive large inputs of terrestrial carbon (C) in the form of dissolved organic matter (DOM). DOM inputs may energetically subsidize heterotrophic bacteria and determine whether lakes function as sources or sinks of atmospheric CO 2 . I experimentally tested this hypothesis using a series of mesocosm experiments in New England lakes. In the first experiment, I observed that CO 2 flux increased by 160% 4 days following a 1,000 μM C addition in the form of DOM. However, this response was relatively short lived, as there was no effect of DOM enrichment on CO 2 flux beyond 8 days. In a second experiment, I demonstrated that peak CO 2 flux from mesocosms in two lakes increased linearly over a broad DOM gradient (slope for both lakes=0.02±0.001 mM CO 2 ·m −2 day −1 per μM DOC, mean±SE). Concomitant changes in bacterial productivity and dissolved oxygen strengthen the inference that increasing CO 2 flux resulted from the metabolism of DOM. I conducted two additional studies to test whether DOM-correlated attributes were responsible for the observed change in plankton metabolism along the subsidy gradient. First, terrestrial DOM reduced light transmittance, but experimental shading revealed that this was not responsible for the observed patterns of CO 2 flux. Second, organically bound nitrogen (N) and phosphorus (P) accompanied DOM inputs, but experimental nutrient additions (without organic C) caused mesocosms to be satuated with CO 2 . Together, these results suggest that C content of terrestrial DOM may be an important subsidy for freshwater bacteria that can influence whether recipient aquatic ecosystems are sources or sinks of atmospheric CO 2 .

Microbial communities can potentially mediate feedbacks between global change and ecosystem funct... more Microbial communities can potentially mediate feedbacks between global change and ecosystem function, owing to their sensitivity to environmental change and their control over critical biogeochemical processes. Numerous ecosystem models have been developed to predict global change effects, but most do not consider microbial mechanisms in detail. In this idea paper, we examine the extent to which incorporation of microbial ecology into ecosystem models improves predictions of carbon (C) dynamics under warming, changes in precipitation regime, and anthropogenic nitrogen (N) enrichment. We focus on three cases in which this approach might be especially valuable: temporal dynamics in microbial responses to environmental change, variation in ecological function within microbial communities, and N effects on microbial activity. Four microbially-based models have addressed these scenarios. In each case, predictions of the microbial-based models differ-sometimes substantially-from comparable conventional models. However, validation and parameterization of model performance is challenging. We recommend that the development of microbial-based models must occur in conjunction with the development of theoretical frameworks that predict the temporal responses of microbial communities, the phylogenetic distribution of microbial functions, and the response of microbes to N enrichment.

† Ashley Shade and Hannes Peter have contributed equally to this work.

The ISME journal, Jan 30, 2015

Viral lysis of microbial hosts releases organic matter that can then be assimilated by nontargete... more Viral lysis of microbial hosts releases organic matter that can then be assimilated by nontargeted microorganisms. Quantitative estimates of virus-mediated recycling of carbon in marine waters, first established in the late 1990s, were originally extrapolated from marine host and virus densities, host carbon content and inferred viral lysis rates. Yet, these estimates did not explicitly incorporate the cascade of complex feedbacks associated with virus-mediated lysis. To evaluate the role of viruses in shaping community structure and ecosystem functioning, we extend dynamic multitrophic ecosystem models to include a virus component, specifically parameterized for processes taking place in the ocean euphotic zone. Crucially, we are able to solve this model analytically, facilitating evaluation of model behavior under many alternative parameterizations. Analyses reveal that the addition of a virus component promotes the emergence of complex communities. In addition, biomass partitioni...

Frontiers in microbiology, 2015

Dormancy is a life history trait that may have important implications for linking microbial commu... more Dormancy is a life history trait that may have important implications for linking microbial communities to the functioning of natural and managed ecosystems. Rapid changes in environmental cues may resuscitate dormant bacteria and create pulses of ecosystem activity. In this study, we used heavy-water (H(18) 2O) stable isotope probing (SIP) to identify fast-growing bacteria that were associated with pulses of trace gasses (CO2, CH4, and N2O) from different ecosystems [agricultural site, grassland, deciduous forest, and coniferous forest (CF)] following a soil-rewetting event. Irrespective of ecosystem type, a large fraction (69-74%) of the bacteria that responded to rewetting were below detection limits in the dry soils. Based on the recovery of sequences, in just a few days, hundreds of rare taxa increased in abundance and in some cases became dominant members of the rewetted communities, especially bacteria belonging to the Sphingomonadaceae, Comamonadaceae, and Oxalobacteraceae. ...

Frontiers in Microbiology, 2014

In ecology, biodiversity-ecosystem functioning (BEF) research has seen a shift in perspective fro... more In ecology, biodiversity-ecosystem functioning (BEF) research has seen a shift in perspective from taxonomy to function in the last two decades, with successful application of trait-based approaches. This shift offers opportunities for a deeper mechanistic understanding of the role of biodiversity in maintaining multiple ecosystem processes and services. In this paper, we highlight studies that have focused on BEF of microbial communities with an emphasis on integrating trait-based approaches to microbial ecology. In doing so, we explore some of the inherent challenges and opportunities of understanding BEF using microbial systems. For example, microbial biologists characterize communities using gene phylogenies that are often unable to resolve functional traits. Additionally, experimental designs of existing microbial BEF studies are often inadequate to unravel BEF relationships. We argue that combining eco-physiological studies with contemporary molecular tools in a trait-based framework can reinforce our ability to link microbial diversity to ecosystem processes. We conclude that such trait-based approaches are a promising framework to increase the understanding of microbial BEF relationships and thus generating systematic principles in microbial ecology and more generally ecology.

The ISME journal, Jan 23, 2014

For any enzyme-catalyzed reaction to occur, the corresponding protein-encoding genes and transcri... more For any enzyme-catalyzed reaction to occur, the corresponding protein-encoding genes and transcripts are necessary prerequisites. Thus, a positive relationship between the abundance of gene or transcripts and corresponding process rates is often assumed. To test this assumption, we conducted a meta-analysis of the relationships between gene and/or transcript abundances and corresponding process rates. We identified 415 studies that quantified the abundance of genes or transcripts for enzymes involved in carbon or nitrogen cycling. However, in only 59 of these manuscripts did the authors report both gene or transcript abundance and rates of the appropriate process. We found that within studies there was a significant but weak positive relationship between gene abundance and the corresponding process. Correlations were not strengthened by accounting for habitat type, differences among genes or reaction products versus reactants, suggesting that other ecological and methodological fact...

The ISME Journal, 2013

Although numerous studies have investigated changes in soil microbial communities across space, q... more Although numerous studies have investigated changes in soil microbial communities across space, questions about the temporal variability in these communities and how this variability compares across soils have received far less attention. We collected soils on a monthly basis (May to November) from replicated plots representing three land-use types (conventional and reduced-input row crop agricultural plots and early successional grasslands) maintained at a research site in Michigan, USA. Using barcoded pyrosequencing of the 16S rRNA gene, we found that the agricultural and early successional land uses harbored unique soil bacterial communities that exhibited distinct temporal patterns. a-Diversity, the numbers of taxa or lineages, was significantly influenced by the sampling month with the temporal variability in a-diversity exceeding the variability between land-use types. In contrast, differences in community composition across landuse types were reasonably constant across the 7-month period, suggesting that the time of sampling is less important when assessing b-diversity patterns. Communities in the agricultural soils were most variable over time and the changes were significantly correlated with soil moisture and temperature. Temporal shifts in bacterial community composition within the successional grassland plots were less predictable and are likely a product of complex interactions between the soil environment and the more diverse plant community. Temporal variability needs to be carefully assessed when comparing microbial diversity across soil types and the temporal patterns in microbial community structure can not necessarily be generalized across land uses, even if those soils are exposed to the same climatic conditions.

PLoS ONE, 2013

There is growing evidence that terrestrial ecosystems are exporting more dissolved organic carbon... more There is growing evidence that terrestrial ecosystems are exporting more dissolved organic carbon (DOC) to aquatic ecosystems than they did just a few decades ago. This ''browning'' phenomenon will alter the chemistry, physics, and biology of inland water bodies in complex and difficult-to-predict ways. Experiments provide an opportunity to elucidate how browning will affect the stability and functioning of aquatic ecosystems. However, it is challenging to obtain sources of DOC that can be used for manipulations at ecologically relevant scales. In this study, we evaluated a commercially available source of humic substances (''Super Hume'') as an analog for natural sources of terrestrial DOC. Based on chemical characterizations, comparative surveys, and whole-ecosystem manipulations, we found that the physical and chemical properties of Super Hume are similar to those of natural DOC in aquatic and terrestrial ecosystems. For example, Super Hume attenuated solar radiation in ways that will not only influence the physiology of aquatic taxa but also the metabolism of entire ecosystems. Based on its chemical properties (high lignin content, high quinone content, and low C:N and C:P ratios), Super Hume is a fairly recalcitrant, low-quality resource for aquatic consumers. Nevertheless, we demonstrate that Super Hume can subsidize aquatic food webs through 1) the uptake of dissolved organic constituents by microorganisms, and 2) the consumption of particulate fractions by larger organisms (i.e., Daphnia). After discussing some of the caveats of Super Hume, we conclude that commercial sources of humic substances can be used to help address pressing ecological questions concerning the increased export of terrestrial DOC to aquatic ecosystems.

A recent analysis revealed that most environmental microbiologists neglect replication in their s... more A recent analysis revealed that most environmental microbiologists neglect replication in their science (Prosser, 2010). Of all peer-reviewed papers published during 2009 in the field's leading journals, slightly more than 70% lacked replication when it came to analyzing microbial community data. The paucity of replication is viewed as an 'endemic' and 'embarrassing' problem that amounts to 'bad science', or worse yet, as the title suggests, lying (Prosser, 2010). Although replication is an important component of experimental design, it is possible to do good science without replication. There are various quantitative techniques -some old, some new -that, when used properly, will allow environmental microbiologists to make strong statistical conclusions from experimental and comparative data. Here, I provide examples where unreplicated data can be used to test hypotheses and yield novel information in a statistically robust manner.

Subsidies are donor-controlled inputs of nutrients and energy that can affect ecosystem-level pro... more Subsidies are donor-controlled inputs of nutrients and energy that can affect ecosystem-level processes in a recipient environment. Lake ecosystems receive large inputs of terrestrial carbon (C) in the form of dissolved organic matter (DOM). DOM inputs may energetically subsidize heterotrophic bacteria and determine whether lakes function as sources or sinks of atmospheric CO 2 . I experimentally tested this hypothesis using a series of mesocosm experiments in New England lakes. In the first experiment, I observed that CO 2 flux increased by 160% 4 days following a 1,000 μM C addition in the form of DOM. However, this response was relatively short lived, as there was no effect of DOM enrichment on CO 2 flux beyond 8 days. In a second experiment, I demonstrated that peak CO 2 flux from mesocosms in two lakes increased linearly over a broad DOM gradient (slope for both lakes=0.02±0.001 mM CO 2 ·m −2 day −1 per μM DOC, mean±SE). Concomitant changes in bacterial productivity and dissolved oxygen strengthen the inference that increasing CO 2 flux resulted from the metabolism of DOM. I conducted two additional studies to test whether DOM-correlated attributes were responsible for the observed change in plankton metabolism along the subsidy gradient. First, terrestrial DOM reduced light transmittance, but experimental shading revealed that this was not responsible for the observed patterns of CO 2 flux. Second, organically bound nitrogen (N) and phosphorus (P) accompanied DOM inputs, but experimental nutrient additions (without organic C) caused mesocosms to be satuated with CO 2 . Together, these results suggest that C content of terrestrial DOM may be an important subsidy for freshwater bacteria that can influence whether recipient aquatic ecosystems are sources or sinks of atmospheric CO 2 .

Microbial communities can potentially mediate feedbacks between global change and ecosystem funct... more Microbial communities can potentially mediate feedbacks between global change and ecosystem function, owing to their sensitivity to environmental change and their control over critical biogeochemical processes. Numerous ecosystem models have been developed to predict global change effects, but most do not consider microbial mechanisms in detail. In this idea paper, we examine the extent to which incorporation of microbial ecology into ecosystem models improves predictions of carbon (C) dynamics under warming, changes in precipitation regime, and anthropogenic nitrogen (N) enrichment. We focus on three cases in which this approach might be especially valuable: temporal dynamics in microbial responses to environmental change, variation in ecological function within microbial communities, and N effects on microbial activity. Four microbially-based models have addressed these scenarios. In each case, predictions of the microbial-based models differ-sometimes substantially-from comparable conventional models. However, validation and parameterization of model performance is challenging. We recommend that the development of microbial-based models must occur in conjunction with the development of theoretical frameworks that predict the temporal responses of microbial communities, the phylogenetic distribution of microbial functions, and the response of microbes to N enrichment.

† Ashley Shade and Hannes Peter have contributed equally to this work.

The ISME journal, Jan 30, 2015

Viral lysis of microbial hosts releases organic matter that can then be assimilated by nontargete... more Viral lysis of microbial hosts releases organic matter that can then be assimilated by nontargeted microorganisms. Quantitative estimates of virus-mediated recycling of carbon in marine waters, first established in the late 1990s, were originally extrapolated from marine host and virus densities, host carbon content and inferred viral lysis rates. Yet, these estimates did not explicitly incorporate the cascade of complex feedbacks associated with virus-mediated lysis. To evaluate the role of viruses in shaping community structure and ecosystem functioning, we extend dynamic multitrophic ecosystem models to include a virus component, specifically parameterized for processes taking place in the ocean euphotic zone. Crucially, we are able to solve this model analytically, facilitating evaluation of model behavior under many alternative parameterizations. Analyses reveal that the addition of a virus component promotes the emergence of complex communities. In addition, biomass partitioni...