Experimental evidence for long-term coexistence of copiotrophic and oligotrophic bacteria in pelagic surface seawater

Most marine copiotrophic bacteria can produce extracellular enzymes to degrade biopolymers into bio-available smaller solutes, while oligotrophic bacteria usually cannot. Bacterial extracellular enzymes and enzymatic products can be a common resource that could be utilized by both copiotrophs and oligotrophs; when present, oligotrophs may outcompete the enzyme-producing copiotrophs. However, copiotrophs and oligotrophs consistently coexist in the ocean. How they maintain coexistence has still not been experimentally studied. In this study, the interaction and coexistence of a copiotroph and an oligotroph, isolated from the same surface seawater sample and utilizing the same proteinaceous substrate, were experimentally investigated. The copiotroph could secrete extracellular proteases to degrade and then utilize the proteinaceous substrate. The oligotroph was unable to utilize the proteinaceous substrate by itself, but could grow by using the hydrolysate amino acids. The copiotroph outcompeted the oligotroph by adsorbing the amino acids quickly and having a higher growth rate in the rich medium. The oligotroph survived by adapting to low concentration of nutrients. The copiotroph and oligotroph were able to maintain long-term (up to 142 days) coexistence in the laboratory. This study indicates that differences in the utilization of different concentrations of nutrients can drive the coexistence of marine copiotrophs and oligotrophs.     

Adaptive genetic traits in pelagic freshwater microbes

Pelagic microbes have adopted distinct strategies to inhabit the pelagial of lakes and oceans and can be broadly categorized in two groups: free-living, specialized oligotrophs and patch-associated generalists or copiotrophs. In this review, we aim to identify genomic traits that enable pelagic freshwater microbes to thrive in their habitat. To do so, we discuss the main genetic differences of pelagic marine and freshwater microbes that are both dominated by specialized oligotrophs and the difference to freshwater sediment microbes, where copiotrophs are more prevalent. We phylogenomically analysed a collection of >7700 metagenome-assembled genomes, classified habitat preferences on different taxonomic levels, and compared the metabolic traits of pelagic freshwater, marine, and freshwater sediment microbes. Metabolic differences are mainly associated with transport functions, environmental information processing, components of the electron transport chain, osmoregulation and the isoelectric point of proteins. Several lineages with known habitat transitions (Nitrososphaeria, SAR11, Methylophilaceae, Synechococcales, Flavobacteriaceae, Planctomycetota) and the underlying mechanisms in this process are discussed in this review. Additionally, the distribution, ecology and genomic make-up of the most abundant freshwater prokaryotes are described in details in separate chapters for Actinobacteriota, Bacteroidota, Burkholderiales, Verrucomicrobiota, Chloroflexota, and ‘Ca. Patescibacteria’.     

In situ determination of kinetic parameters for biofilms: Isolation and characterization of oligotrophic biofilms

This article develops and utilizes an in situ technique to estimate the Monod half-maximum rate concentration, K(s) and the maximum specific utilization rate constant, k, for biofilms. The technique employs a curve-matching method with kinetic results from several short-term experiments with completely mixed biofilm reactors. Use of the in situ method eliminates the two drawbacks of using conventional suspended-growth measurements to characterize biofilm: possible alteration of cell physiology and a major investment to run the suspended-growth tests. Results with five cultures of biofilm-forming oligotrophs demonstrated the in situ technique and supported the hypothesis that K(s) values were lower for the biofilm oligotrophs than for typical copiotrophs.     

Mechanistic model of nutrient uptake explains dichotomy between marine oligotrophic and copiotrophic bacteria

Marine bacterial diversity is immense and believed to be driven in part by trade-offs in metabolic strategies. Here we consider heterotrophs that rely on organic carbon as an energy source and present a molecular-level model of cell metabolism that explains the dichotomy between copiotrophs—which dominate in carbon-rich environments—and oligotrophs—which dominate in carbon-poor environments—as the consequence of trade-offs between nutrient transport systems. While prototypical copiotrophs, like Vibrios, possess numerous phosphotransferase systems (PTS), prototypical oligotrophs, such as SAR11, lack PTS and rely on ATP-binding cassette (ABC) transporters, which use binding proteins. We develop models of both transport systems and use them in proteome allocation problems to predict the optimal nutrient uptake and metabolic strategy as a function of carbon availability. We derive a Michaelis–Menten approximation of ABC transport, analytically demonstrating how the half-saturation concentration is a function of binding protein abundance. We predict that oligotrophs can attain nanomolar half-saturation concentrations using binding proteins with only micromolar dissociation constants and while closely matching transport and metabolic capacities. However, our model predicts that this requires large periplasms and that the slow diffusion of the binding proteins limits uptake. Thus, binding proteins are critical for oligotrophic survival yet severely constrain growth rates. We propose that this trade-off fundamentally shaped the divergent evolution of oligotrophs and copiotrophs.     

The evolving copiotrophic/oligotrophic dichotomy: From Winogradsky to physiology and genomics

Nearly 100 years ago, Winogradsky published a classic communication in which he described two groups of microbes, zymogenic and autochthonous. When organic matter penetrates the soil, zymogenic microbes quickly multiply and degrade it, then giving way to the slow combustion of autochthonous microbes. Although the text was originally written in French, it is often cited by English-speaking authors. We undertook a complete translation of the 1924 publication, which we provide as Supporting information. Here, we introduce the translation and describe how the zymogenic/autochthonous dichotomy shaped research questions in the study of microbial diversity and physiology. We also identify in the literature three additional and closely related dichotomies, which we propose to call exclusive copiotrophs/oligotrophs, coexisting copiotrophs/oligotrophs and fast-growing/slow-growing microbes. While Winogradsky focussed on a successional view of microbial populations over time, the current discussion is focussed on the differences in the specific growth rate of microbes as a function of the concentration of a given limiting substrate. In the future, it will be relevant to keep in mind both nutrient-focussed and time-focussed microbial dichotomies and to design experiments with both isolated laboratory cultures and multi-species communities in the spirit of Winogradsky's direct method.     

Life-history strategies of soil microbial communities in an arid ecosystem

The overwhelming taxonomic diversity and metabolic complexity of microorganisms can be simplified by a life-history classification; copiotrophs grow faster and rely on resource availability, whereas oligotrophs efficiently exploit resource at the expense of growth rate. Here, we hypothesize that community-level traits inferred from metagenomic data can distinguish copiotrophic and oligotrophic microbial communities. Moreover, we hypothesize that oligotrophic microbial communities harbor more unannotated genes. To test these hypotheses, we conducted metagenomic analyses of soil samples collected from copiotrophic vegetated areas and from oligotrophic bare ground devoid of vegetation in an arid-hyperarid region of the Sonoran Desert, Arizona, USA. Results supported our hypotheses, as we found that multiple ecologically informed life-history traits including average 16S ribosomal RNA gene copy number, codon usage bias in ribosomal genes and predicted maximum growth rate were higher for microbial communities in vegetated than bare soils, and that oligotrophic microbial communities in bare soils harbored a higher proportion of genes that are unavailable in public reference databases. Collectively, our work demonstrates that life-history traits can distill complex microbial communities into ecologically coherent units and highlights that oligotrophic microbial communities serve as a rich source of novel functions.Subject terms: Microbial ecology, Community ecology     

Bacterial Community Structure in Relation to the Carbon Environments in Lettuce and Tomato Rhizospheres and in Bulk Soil

Abstract Crop roots provide dynamic nutrient environments within agroecosystems that can influence the relative abundance and activity of oligotrophic and copiotrophic microorganisms. Copiotrophic organisms grow in carbon (C)-rich environments and their distribution implies that C abundance favors their survival. Survival of oligotrophic organisms is dependent on their ability to multiply and maintain activity in habitats of low C flux. To determine if spatial variation in available C along the root coincides with different physiological groups of bacteria, we isolated bacteria from the rhizosphere at different locations along the tap root of lettuce and tomato plants grown under greenhouse and field conditions. In all five experiments, the overall numbers of both oligotrophs and copiotrophs were high at the upper portions of the root and lower at tip locations and in the bulk soil environment. Consistent patterns in the ratio of copiotrophic to oligotrophic (C:O) bacteria along the roots of lettuce and tomato were obtained and clearly showed that the C:O ratio was different for these two crop species. With lettuce, C:O ratios were high at the root tip (1.22 to 1.61) and upper mid-root locations (0.90 to 1.30), intermediate at the lower mid-root locations (0.73 to 0.95), and low at the root base (0.56 to 0.76). With tomato, C:O ratios were low at root tip locations (0.50 to 0.68) and high at mid and base locations along the root (1.20 to 1.28). These differences may reflect qualitative and quantitative differences in root exudates between these crop species. In our experiments, nitrogen (N) concentrations and lateral branch sites, providing C sources, were important factors influencing bacterial populations in the rhizosphere of lettuce and tomato. Competitive interactions between microorganisms and physiological constraints with respect to substrate affinity may be two important mechanisms influencing bacterial populations and structure of rhizosphere communities. Received: 14 August 1996; Accepted: 10 December 1996     

Cell size,genome size,and maximum growth rate are near‐independent dimensions of ecological variation across bacteria and archaea

Among bacteria and archaea, maximum relative growth rate, cell diameter, and genome size are widely regarded as important influences on ecological strategy. Via the most extensive data compilation so far for these traits across all clades and habitats, we ask whether they are correlated and if so how. Overall, we found little correlation among them, indicating they should be considered as independent dimensions of ecological variation. Nor was correlation evident within particular habitat types. A weak nonlinearity (6% of variance) was found whereby high maximum growth rates (temperature‐adjusted) tended to occur in the midrange of cell diameters. Species identified in the literature as oligotrophs or copiotrophs were clearly separated on the dimension of maximum growth rate, but not on the dimensions of genome size or cell diameter.     

Secondary osteon size and collagen/lamellar organization (“osteon morphotypes”) are not coupled,but potentially adapt independently for local strain mode or magnitude

In bone, matrix slippage that occurs at cement lines of secondary osteons during loading is an important toughening mechanism. Toughness can also be enhanced by modifications in osteon cross-sectional size (diameter) for specific load environments; for example, smaller osteons in more highly strained “compression” regions vs. larger osteons in less strained “tension” regions. Additional osteon characteristics that enhance toughness are distinctive variations in collagen/lamellar organization (i.e., “osteon morphotypes”). Interactions might exist between osteon diameter and morphotype that represent adaptations for resisting deleterious shear stresses that occur at the cement line. This may be why osteons often have a peripheral ring (or “hoop”) of highly oblique/transverse collagen. We hypothesized that well developed/distinct “hoops” are compensatory adaptations in cases where increased osteon diameter is mechanically advantageous (e.g., larger osteons in “tension” regions would have well developed/distinct “hoops” in order to resist deleterious consequences of co-existing localized shear stresses). We tested this hypothesis by determining if there are correlations between osteon diameters and strongly hooped morphotypes in “tension”, “compression”, and “neutral axis” regions of femora (chimpanzees, humans), radii (horse, sheep) and calcanei (horse, deer). The results reject the hypothesis—larger osteons are not associated with well developed/distinct “hoops”, even in “tension regions” where the effect was expected to be obvious. Although osteon diameter and morphotype are not coupled, osteon diameters seem to be associated with increased strain magnitudes in some cases, but this is inconsistent. By contrast, osteon morphotypes are more strongly correlated with the distribution of tension and compression.     

Isolation and Partial Characterization of Bacterial Strains on Low Organic Carbon Medium from Soils Fertilized with Different Organic Amendments

A total of 720 bacterial strains were isolated from soils with four different organic amendment regimes on a low organic carbon (low-C) agar medium (10 µg C ml^?1) traditionally used for isolation of oligotrophs. Organic amendments in combination with field history resulted in differences in dissolved organic carbon contents in these soils. There were negative correlations between total and dissolved organic carbon content and the number of isolates on low-C agar medium, whereas these correlations were absent for bacterial strains isolated from the same soil on high-C agar medium (1,000 µg C ml^?1). Repeated transfers (up to ten times) of the isolates from low-C agar medium to fresh low- and high-C agar media were done to test for exclusive growth under oligotrophic conditions. The number of isolates exclusively growing under oligotrophic conditions dropped after each subsequent transfer from 241 after the first to 98 after the third transfer step. Identification on the basis of partial 16S rRNA gene sequences revealed that most of the 241 isolates (as well as the subset of 98 isolates) belong to widespread genera such as Streptomyces, Rhizobium, Bradyrhizobium, and Mesorhizobium, and the taxonomic composition of dominant genera changed from the first transfer step to the third. A selected subset of 17 isolates were further identified and characterized for exclusive growth on low-C agar medium. Two isolates continued to grow only on low-C agar medium up to the tenth transfer step and matched most closely with Rhizobium sullae and an uncultured bacterium on the basis of the almost full-length 16S rRNA gene. It was concluded that the vast majority of strains which are isolated on low-C agar media belong to the trophic group of microorganisms adapted to a “broad range” of carbon concentrations, including well-known and widespread bacterial genera. Oligotrophy is a physiological, not a taxonomic property, and can only be identified by cultural means so far. We showed that true oligotrophs that are unable to grow on high carbon media are rare and belong to genera that also contain broad-range and copiotrophic strains.     

Microbial cultivation and the role of microbial resource centers in the omics era

Despite tremendous advances in microbial ecology over the past two decades, traditional cultivation methods have failed to grow ecologically more relevant microorganisms in the laboratory, leading to a predominance of weed-like species in the world’s culture collections. In this review, we highlight the gap between culture-based and culture-independent methods of microbial diversity analysis, especially in investigations of slow growers, oligotrophs, and fastidious and recalcitrant microorganisms. Furthermore, we emphasize the importance of microbial cultivation and the acquisition of the cultivation-based phenotypic data for the testing of hypotheses arising from genomics and proteomics approaches. Technical difficulties in cultivating novel microorganisms and how modern approaches have helped to overcome these limitations are highlighted. After cultivation, adequate preservation without changes in genotypic and phenotypic features of these microorganisms is necessary for future research and training. Hence, the contribution of microbial resource centers in the handling, preservation, and distribution of this novel diversity is discussed. Finally, we explore the concept of microbial patenting and requisite guidelines of the “Budapest Treaty” for establishment of an International Depositary Authority.     

Causal mechanisms of evolution and the capacity for niche construction

Ernst Mayr proposed a distinction between “proximate”, mechanistic, and “ultimate”, evolutionary, causes of biological phenomena. This dichotomy has influenced the thinking of many biologists, but it is increasingly perceived as impeding modern studies of evolutionary processes, including study of “niche construction” in which organisms alter their environments in ways supportive of their evolutionary success. Some still find value for this dichotomy in its separation of answers to “how?” versus “why?”questions about evolution. But “why is A?” questions about evolution necessarily take the form “how does A occur?”, so this separation is illusory. Moreover, the dichotomy distorts our view of evolutionary causality, in that, contra Mayr, the action of natural selection, driven by genotype-phenotype-environment interactions which constitute adaptations, is no less “proximate” than the biological mechanisms which are altered by naturally selected genetic variants. Mayr’s dichotomy thus needs replacement by more realistic, mechanistic views of evolution. From a mechanistic viewpoint, there is a continuum of adaptations from those evolving as responses to unchanging environmental pressures to those evolving as the capacity for niche construction, and intermediate stages of this can be identified. Some biologists postulate an association of “phenotypic plasticity” (phenotype-environment covariation with genotype held constant) with capacity for niche construction. Both “plasticity” and niche construction comprise wide ranges of adaptive mechanisms, often fully heritable and resulting from case-specific evolution. Association of “plasticity” with niche construction is most likely to arise in systems wherein capacity for complex learning and behavioral flexibility have already evolved.     

Sodium—A Functional Plant Nutrient

Plant scientists usually classify plant mineral nutrients based on the concept of “essentiality” defined by Arnon and Stout as those elements necessary to complete the life cycle of a plant. Certain other elements such as Na have a ubiquitous presence in soils and waters and are widely taken up and utilized by plants, but are not considered as plant nutrients because they do not meet the strict definition of “essentiality.” Sodium has a very specific function in the concentration of carbon dioxide in a limited number of C₄ plants and thus is essential to these plants, but this in itself is insufficient to generalize that Na is essential for higher plants. The unique set of roles that Na can play in plant metabolism suggests that the basic concept of what comprises a plant nutrient should be reexamined. We contend that the class of plant mineral nutrients should be comprised not only of those elements necessary for completing the life cycle, but also those elements which promote maximal biomass yield and/or which reduce the requirement (critical level) of an essential element. We suggest that nutrients functioning in this latter manner should be termed “functional nutrients.” Thus plant mineral nutrients would be comprised of two major groups, “essential nutrients” and “functional nutrients.” We present an array of evidence and arguments to support the classification of Na as a “functional nutrient,” including its requirement for maximal biomass growth for many plants and its demonstrated ability to replace K in a number of ways, such as being an osmoticium for cell enlargement and as an accompanying cation for long-distance transport. Although in this paper we have only attempted to make the case for Na being a “functional nutrient,” other elements such as Si and Se may also confirm to the proposed category of “functional nutrients.”     

Evidence of an evolutionary‐developmental trade‐off between drag avoidance and tolerance strategies in wave‐swept intertidal kelps (Laminariales,Phaeophyceae)

Kelps are a clade of morphologically diverse, ecologically important habitat‐forming species. Many kelps live in wave‐swept environments and are exposed to chronic flow‐induced stress. In order to grow and survive in these harsh environments, kelps can streamline (reducing drag coefficient) to avoid drag or to increase attachment and breakage force to tolerate it. We aimed to quantify the drag tolerance and streamlining strategies of kelps from wave‐swept intertidal habitats. We measured drag coefficient and tenacity of populations from eight kelp species over a wide range of sizes to determine whether kelps avoid dislodgement by reducing drag coefficient or by increasing tenacity as they grow, and whether these traits are traded off. We employed phylogenetic comparative methods to rule out potentially confounding effects of species' relatedness. There was a significant negative relationship between drag avoidance and tolerance strategies, even after incorporating phylogeny. Kelps that were more tenacious were less able to reduce drag, resulting in a continuum from “tolerators” to “streamliners,” with some species demonstrating intermediate, mixed strategies. Drag and tenacity were correlated with geometric properties (i.e., second moment of area) of the stipe in large kelps. Results presented in this study suggest that kelps are either strong or streamlined, but not both. This continuum is consistent with avoidance and tolerance trade‐offs that have been documented in many different biological systems and may have widespread implications for the evolution of large macroalgae, perhaps driving morphological diversity within this group.     

Using a “time machine” to test for local adaptation of aquatic microbes to temporal and spatial environmental variation

Local adaptation occurs when different environments are dominated by different specialist genotypes, each of which is relatively fit in its local conditions and relatively unfit under other conditions. Analogously, ecological species sorting occurs when different environments are dominated by different competing species, each of which is relatively fit in its local conditions. The simplest theory predicts that spatial, but not temporal, environmental variation selects for local adaptation (or generates species sorting), but this prediction is difficult to test. Although organisms can be reciprocally transplanted among sites, doing so among times seems implausible. Here, we describe a reciprocal transplant experiment testing for local adaptation or species sorting of lake bacteria in response to both temporal and spatial variation in water chemistry. The experiment used a –80°C freezer as a “time machine.” Bacterial isolates and water samples were frozen for later use, allowing transplantation of older isolates “forward in time” and newer isolates “backward in time.” Surprisingly, local maladaptation predominated over local adaptation in both space and time. Such local maladaptation may indicate that adaptation, or the analogous species sorting process, fails to keep pace with temporal fluctuations in water chemistry. This hypothesis could be tested with more finely resolved temporal data.     

ENVIRONMENTAL SENSITIVITY OF SEXUAL AND APOMICTIC ANTENNARIA: DO APOMICTS HAVE GENERAL-PURPOSE GENOTYPES?

The fact that apomictic taxa typically occupy a wider range of environments than their sexual relatives has generated the hypothesis that apomicts are more likely to possess “general-purpose genotypes,” i.e., genotypes whose performance is relatively insensitive to changes in environmental conditions. This hypothesis was tested by cloning sexual and apomictic females of Antennaria parvifolia (Asteraceae) and growing each genotype in six growth-chamber environments varying in temperature and moisture levels. A joint regression analysis revealed that the survival of apomictic genotypes was significantly less sensitive to environmental conditions than that of sexual genotypes but demonstrated no differences with regard to flowering or biomass. However, the coefficient of variation in biomass across the six environments was significantly lower for apomicts than for sexuals, and the geometric mean of survival over the six environments was significantly higher for apomicts. Apomicts significantly exceeded sexuals in mean survival, mean flower-head production, and mean biomass. These results support the hypothesis that apomictic genotypes are more “general-purpose” than sexuals, and increase the difficulty of explaining the persistence of sexual reproduction in A. parvifolia.     

Screening of carbon dioxide-requiring extreme oligotrophs from soil

We screened soil samples for CO(2)-requiring extreme oligotrophs similar to Rhodococcus erythropolis N9T-4, which can grow on a basal salt agar medium without an organic carbon source. From 387 soil samples, three isolates were obtained and identified as Streptomyces spp. by 16S rDNA analysis. The isolates required gaseous CO(2) for growth and grew on a basal salt medium solidified by silica gel. These results suggest that such CO(2)-requiring oligotrophs occur widely in nature.     

The past explains the present: Emotional adaptations and the structure of ancestral environments

Present conditions and selection pressures are irrelevant to the present design of organisms and do not explain how or why organisms behave adaptively, when they do. To whatever non-chance extent organisms are behaving adaptively, it is 1) because of the operation of underlying adaptations whose present design is the product of selection in the past, and 2) because present conditions resemble past conditions in those specific ways made developmentally and functionally important by the design of those adaptations. All adaptations evolved in response to the repeating elements of past environments, and their structure reflects in detail the recurrent structure of ancestral environments. Even planning mechanisms (such as “consciousness”), which supposedly deal with novel situations, depend on ancestrally shaped categorization processes and are therefore not free of the fast. In fact, the categorization of each new situation into evolutionarily repeating classes involves another kind of adaptation, the emotions, which match specialized modes of organismic operation to evolutionarily recurrent situations. The detailed statistical structure of these iterated systems of events is reflected in the detailed structure of the algorithms that govern emotional state. For this reason, the system of psychological adaptations that comprises each individual meets the present only as a version of the past.