Cross-feeding, the exchange of nutrients between organisms, is ubiquitous in microbial communities. Despite its importance in natural and engineered microbial systems, our understanding of how inter-species cross-feeding arises is incomplete, with existing theories limited to specific scenarios. Here, we introduce a novel theory for the emergence of such cross-feeding, which we term noise-averaging cooperation (NAC). NAC is based on the idea that, due to their small size, bacteria are prone to noisy regulation of metabolism which limits their growth rate. To compensate, related bacteria can share metabolites with each other to ‘average out’ noise and improve their collective growth. According to the Black Queen Hypothesis, this metabolite sharing among kin, a form of ‘leakage’, then allows for the evolution of metabolic interdependencies among species including de novo speciation via gene deletions. We first characterize NAC in a simple ecological model of cell metabolism, showing that metabolite leakage can in principle substantially increase growth rate in a community context. Next, we develop a generalized framework for estimating the potential benefits of NAC among real bacteria. Using single-cell protein abundance data, we predict that bacteria suffer from substantial noise-driven growth inefficiencies, and may therefore benefit from NAC. We then discuss potential evolutionary pathways for the emergence of NAC. Finally, we review existing evidence for NAC and outline potential experimental approaches to detect NAC in microbial communities.
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Emergence of sector and spiral patterns from a two-species mutualistic cross-feeding model
The ubiquitous existence of microbial communities marks the importance of understanding how species interact within the community to coexist and their spatial organization. We study a two-species mutualistic cross-feeding model through a stochastic cellular automaton on a square lattice using kinetic Monte Carlo simulation. Our model encapsulates the essential dynamic processes such as cell growth, and nutrient excretion, diffusion and uptake. Focusing on the interplay among nutrient diffusion and individual cell division, we discover three general classes of colony morphology: co-existing sectors, co-existing spirals, and engulfment. When the cross-feeding nutrient is widely available, either through high excretion or fast diffusion, a stable circular colony with alternating species sector emerges. When the consumer cells rely on being spatially close to the producers, we observe a stable spiral. We also see one species being engulfed by the other when species interfaces merge due to stochastic fluctuation. By tuning the diffusion rate and the growth rate, we are able to gain quantitative insights into the structures of the sectors and the spirals.
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- NSF-PAR ID:
- 10376111
- Editor(s):
- Csikász-Nagy, Attila
- Date Published:
- Journal Name:
- PLOS ONE
- Volume:
- 17
- Issue:
- 10
- ISSN:
- 1932-6203
- Page Range / eLocation ID:
- e0276268
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Abstract Biogeochemical cycling has often been characterized by physical and microbial processes, yet animals can be essential mediators of energy and nutrients in ecosystems. Excretion by aggregated animals can be an important local source of inorganic nutrients in green food webs; however, whether animals are a source of dissolved energy that can support brown food webs is understudied.
We tested whether animal aggregations are a substantial flux of bioavailable dissolved organic matter (DOM) by studying spatially stable, biogeochemical hotspots formed by filter‐feeding freshwater mussels. We used parallel‐factor analysis to quantify DOM fluorescent components composition of mussel excretion and expected digestive breakdown of particulate food sources would lead to excretion of labile DOM. Next, we combined measured excretion rates of DOM, ammonium (
, N) and phosphorous (SRP; P) for 22 species with biomass estimates for 14 aggregations to quantify contributions of DOM, N and P to local availability. Because mussels occupy distinct stoichiometric niches, we anticipated that differences in species biomass and assemblage structure would elicit different flux and stoichiometries of aggregate excretion. Aggregate dissolved organic carbon (DOC) excretion was minor (1%–11%) compared to N (12%–2,860%) and P (1%–97%), yet generalities across assemblages emerged regarding organic matter transformation by mussels towards labile protein‐like compounds compared to abundant aromatic, humic compounds in ambient water.
Aggregate excretion of labile DOM was a substantial pool of bioavailable energy, contributing 2%–114% of local labile DOM. Spatial differences in assemblage structure led to strong differences in aggregate flux and stoichiometry driven by biomass and stoichiometric trait expression of species with contrasting dominance patterns.
Under the nutrient conditions of our study (high C:nutrient), biogeochemical hotspots associated with low‐trophic position animal biomass may indirectly control energy flow to the brown food web by shifting C:nutrient stoichiometry available to microbes or directly by increasing the flux of microbially available DOM. Collectively, our results highlight a potentially substantial flux of labile energy and nutrients to microbial communities through the transformation of ingested organic matter by aggregations of animals and emphasize that shared functional trait classification may not translate into shared ecological function.
A free
Plain Language Summary can be found within the Supporting Information of this article. -
Dubilier, Nicole (Ed.)more » « less
ABSTRACT Prochlorococcus is an abundant photosynthetic bacterium in the open ocean, where nitrogen (N) often limits phytoplankton growth. In the low-light-adapted LLI clade ofProchlorococcus , nearly all cells can assimilate nitrite (NO2−), with a subset capable of assimilating nitrate (NO3−). LLI cells are maximally abundant near the primary NO2−maximum layer, an oceanographic feature that may, in part, be due to incomplete assimilatory NO3−reduction and subsequent NO2−release by phytoplankton. We hypothesized that someProchlorococcus exhibit incomplete assimilatory NO3−reduction and examined NO2−accumulation in cultures of threeProchlorococcus strains (MIT0915, MIT0917, and SB) and twoSynechococcus strains (WH8102 and WH7803). Only MIT0917 and SB accumulated external NO2−during growth on NO3−. Approximately 20–30% of the NO3−transported into the cell by MIT0917 was released as NO2−, with the rest assimilated into biomass. We further observed that co-cultures using NO3−as the sole N source could be established for MIT0917 andProchlorococcus strain MIT1214 that can assimilate NO2−but not NO3−. In these co-cultures, the NO2−released by MIT0917 is efficiently consumed by its partner strain, MIT1214. Our findings highlight the potential for emergent metabolic partnerships that are mediated by the production and consumption of N cycle intermediates withinProchlorococcus populations.IMPORTANCE Earth’s biogeochemical cycles are substantially driven by microorganisms and their interactions. Given that N often limits marine photosynthesis, we investigated the potential for N cross-feeding within populations of
Prochlorococcus , the numerically dominant photosynthetic cell in the subtropical open ocean. In laboratory cultures, someProchlorococcus cells release extracellular NO2−during growth on NO3−. In the wild,Prochlorococcus populations are composed of multiple functional types, including those that cannot use NO3−but can still assimilate NO2−. We show that metabolic dependencies arise whenProchlorococcus strains with complementary NO2−production and consumption phenotypes are grown together on NO3−. These findings demonstrate the potential for emergent metabolic partnerships, possibly modulating ocean nutrient gradients, that are mediated by cross-feeding of N cycle intermediates. -
Functional traits are characteristics of an organism that represent how it interacts with its environment and can influence the structure and function of ecosystems. Ecological stoichiometry provides a framework to understand ecosystem structure and function by modeling the coupled flow of elements (e.g. carbon [C], nitrogen [N], phosphorus [P]) between consumers and their environment. Animals tend to be homeostatic in their nutrient requirements and preferentially sequester the element in shortest supply relative to demand, and release relatively more of the element in excess. Tissue stoichiometry is an important functional trait that allows for predictions among the elemental composition of animals, their diet, and their waste products, with important effects on the cycling and availability of nutrients in ecosystems. Here we examined the tissue stoichiometric niches (C:N:P) and nutrient recycling stoichiometries (N:P) of several filter‐feeding freshwater mussels in the subfamily Ambleminae. Despite occupying the same functional‐feeding group and being restricted to a single subfamily‐level radiation, we found that species occupied distinct stoichiometric niches and that these niches varied, in part, as a function of their evolutionary history. The relationship between phylogenetic divergence and functional divergence suggests that evolutionary processes may be shaping niche complementarity and resource partitioning. Tissue and excretion stoichiometry were negatively correlated as predicted by stoichiometric theory. When scaled to the community, higher species richness and phylogenetic diversity resulted in greater functional evenness and reduced functional dispersion. Filter‐feeding bivalves are an ecologically important guild in freshwater ecosystems globally, and our study provides a more nuanced view of the stoichiometric niches and ecological functions performed by this phylogenetically and ecologically diverse assemblage.more » « less
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Abstract Interactive microbial communities are ubiquitous, influencing biogeochemical cycles and host health. One widespread interaction is nutrient exchange, or cross-feeding, wherein metabolites are transferred between microbes. Some cross-fed metabolites, such as vitamins, amino acids, and ammonium (NH4+), are communally valuable and impose a cost on the producer. The mechanisms that enforce cross-feeding of communally valuable metabolites are not fully understood. Previously we engineered a cross-feeding coculture between N2-fixing Rhodopseudomonas palustris and fermentative Escherichia coli. Engineered R. palustris excretes essential nitrogen as NH4+ to E. coli, while E. coli excretes essential carbon as fermentation products to R. palustris. Here, we sought to determine whether a reciprocal cross-feeding relationship would evolve spontaneously in cocultures with wild-type R. palustris, which is not known to excrete NH4+. Indeed, we observed the emergence of NH4+ cross-feeding, but driven by adaptation of E. coli alone. A missense mutation in E. coli NtrC, a regulator of nitrogen scavenging, resulted in constitutive activation of an NH4+ transporter. This activity likely allowed E. coli to subsist on the small amount of leaked NH4+ and better reciprocate through elevated excretion of fermentation products from a larger E. coli population. Our results indicate that enhanced nutrient uptake by recipients, rather than increased excretion by producers, is an underappreciated yet possibly prevalent mechanism by which cross-feeding can emerge.
- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1371/journal.pone.0276268
