Biology subjects

McCully, A. L.

Publications and source records attributed to McCully, A. L..

3 recordsLinked to original sources

bioRxiv2018

An Escherichia coli nitrogen starvation response is important for mutualistic coexistence with Rhodopseudomonas palustris

Microbial mutualistic cross-feeding interactions are ubiquitous and can drive important community functions. Engaging in cross-feeding undoubtedly affects the physiology and metabolism of individual species involved. However, the nature in which an individuals physiology is influenced by cross-feeding and the importance of those physiological changes for the mutualism have received little attention. We previously developed a genetically tractable coculture to study bacterial mutualisms. The coculture consists of fermentative Escherichia coli and phototrophic Rhodopseudomonas palustris. In this coculture, E. coli anaerobically ferments sugars into excreted organic acids as a carbon source for R. palustris. In return, a genetically-engineered R. palustris constitutively converts N2 into NH4+, providing E. coli with essential nitrogen. Using RNA-seq and proteomics, we identified transcript and protein levels that differ in each partner when grown in coculture versus monoculture. When in coculture with R. palustris, E. coli gene-expression changes resembled a nitrogen starvation response under the control of the transcriptional regulator NtrC. By genetically disrupting E. coli NtrC, we determined that a nitrogen starvation response is important for a stable coexistence, especially at low R. palustris NH4+ excretion levels. Destabilization of the nitrogen starvation regulatory network resulted in variable growth trends and in some cases, extinction. Our results highlight that alternative physiological states can be important for survival within cooperative cross-feeding relationships.\n\nImportanceMutualistic cross-feeding between microbes within multispecies communities is widespread. Studying how mutualistic interactions influence the physiology of each species involved is important for understanding how mutualisms function and persist in both natural and applied settings. Using a bacterial mutualism consisting of Rhodopseudomonas palustris and Escherichia coli growing cooperatively through bidirectional nutrient exchange, we determined that an E. coli nitrogen starvation response is important for maintaining a stable coexistence. The lack of an E. coli nitrogen starvation response ultimately destabilized the mutualism and, in some cases, led to community collapse after serial transfers. Our findings thus inform on the potential necessity of an alternative physiological state for mutualistic coexistence with another species compared to the physiology of species grown in isolation.

microbiology↗

bioRxiv2017

Recipient-Biased Competition For A Cross-Fed Nutrient Is Required For Coexistence Of Microbial Mutualists

Many mutualistic microbial relationships are based on nutrient cross-feeding. Traditionally, cross-feeding is viewed as being unidirectional from the producer to the recipient. This is likely true when a producers metabolic waste, such as fermentation products, provides carbon for a recipient. However, in some cases the cross-fed nutrient holds value for both the producer and the recipient. In such cases, there is potential for nutrient reacquisition by producer cells in a population, leading to competition against recipients. Here we investigate the consequences of inter-partner competition for cross-fed nutrients on mutualism dynamics using an anaerobic coculture pairing fermentative Escherichia coli and phototrophic Rhodopseudomonas palustris. In this coculture, E. coli excretes waste organic acids that provide carbon for R. palustris. In return, R. palustris cross-feeds E. coli ammonium (NH4+), a valuable nitrogen compound that both species prefer. To explore the potential for inter-partner competition, we first used a kinetic model to simulate cocultures with varied affinities for NH4+ in each species. The model predicted that inter-partner competition for cross-fed NH4+ could profoundly impact population dynamics. We then experimentally tested the predictions by culturing mutants lacking NH4+ transporters in both NH4+ competition assays and cooperative cocultures. Both theoretical and experimental results indicated that the recipient must have a competitive advantage in acquiring valuable cross-fed NH4+ to avoid collapse of the mutualism. Thus, the very metabolites that form the basis for cooperative cross-feeding can also be subject to competition between mutualistic partners.\n\nSignificanceMutualistic relationships, particularly those based on nutrient cross-feeding, promote stability of diverse ecosystems and drive global biogeochemical cycles. Cross-fed nutrients within these systems can be either waste products valued only by one partner or nutrients that both partners value. Here, we explore how inter-partner competition for a communally-valuable cross-fed nutrient impacts mutualism dynamics. We discovered that mutualism stability necessitates that the recipient have a competitive advantage against the producer in obtaining the cross-fed nutrient. We propose that the requirement for recipient-biased competition is a general rule for mutualistic coexistence based on the transfer of communally valuable resources, microbial or otherwise.

microbiology↗

bioRxiv2016

Growth-independent cross-feeding modifies boundaries for coexistence in a bacterial mutualism

Nutrient cross-feeding can stabilize microbial mutualisms, including those important for carbon cycling in nutrient-limited anaerobic environments. It remains poorly understood how nutrient limitation within natural environments impacts mutualist growth, cross-feeding levels, and ultimately mutualism dynamics. We examined the effects of nutrient limitation within a mutualism using theoretical and experimental approaches with a synthetic anaerobic coculture pairing fermentative Escherichia coli and phototrophic Rhodopseudomonas palustris. In this coculture, E. coli and R. palustris resemble an anaerobic food web by cross-feeding essential carbon (organic acids) and nitrogen (ammonium), respectively. Organic acid cross-feeding stemming from E. coli fermentation can continue in a growth-independent manner during nutrient limitation, while ammonium cross-feeding by R. palustris is growth-dependent. When ammonium cross-feeding was limited, coculture trends changed yet coexistence persisted under both homogenous and heterogenous conditions. Theoretical modeling indicated that growth-independent fermentation was crucial to sustain cooperative growth under conditions of low nutrient exchange. We also show that growth-independent fermentation sets the upper E. coli cell density at which this mutualism is supported. Thus, growth-independent fermentation can conditionally stabilize or destabilize a mutualism, indicating the potential importance of growth-independent metabolism for nutrient-limited mutualistic communities.\n\nConflict of interestThe authors declare no conflict of interest.

microbiology↗