Phylosymbiosis is a pattern defined as the tendency of closely related species to host microbiota whose compositions resemble each other more than host species drawn at random from the same tree. Understanding the mechanisms behind phylosymbiosis is important because it can shed light on rules governing the assembly of host-associated microbiotas and, potentially, their coevolutionary dynamics with hosts. For example, is phylosymbiosis a result of coevolution, or can it be generated by simple ecological filtering processes? Beyond qualitative theoretical models, quantitative theoretical expectations can provide new insights. For example, deviations from a simple baseline of ecological filtering may be used to test more-complex hypotheses (e.g., coevolution). Here, we use simulations to provide evidence that simple host-related ecological filtering can readily generate phylosymbiosis, and we contrast these predictions with real-world data. We find that while phylosymbiosis is widespread in nature, phylosymbiosis patterns are compatible with a simple ecological model in the majority of taxa. Internal compartments of hosts, such as the animal gut, often display stronger phylosymbiosis than expected from a purely ecological filtering process, suggesting that other mechanisms are also involved.
Marine microbes exhibit seasonal cycles in community composition, yet the key drivers of these patterns and microbial population fidelity to specific environmental conditions remain to be determined. To begin addressing these questions, we characterized microbial dynamics weekly for 3 years at a temperate, coastal site with dramatic environmental seasonality. This high-resolution time series reveals that changes in microbial community composition are not continuous; over the duration of the time series, the community instead resolves into distinct summer and winter profiles with rapid spring and fall transitions between these states. Here, we show that these community shifts involve switching between closely related strains that exhibit either summer or winter preferences. Moreover, taxa repeat this process annually in both this and another temperate coastal time series, suggesting that this phenomenon may be widespread in marine ecosystems. To address potential biogeochemical impacts of these community changes, PICRUSt-based metagenomes predict seasonality in transporters, photosynthetic proteins, peptidases and carbohydrate metabolic pathways in spite of closely related summer- and winter-associated taxa. Thus, even small temperature shifts, such as those predicted by climate change models, could affect both the structure and function of marine ecosystems.
There is a growing recognition of the roles of marine microenvironments as reservoirs of biodiversity and as sites of enhanced biological activity and in facilitating biological interactions. Here, we examine the bacterial community inhabiting free-living and particle-associated seawater microenvironments at the Pivers Island Coastal Observatory (PICO). 16S rRNA gene libraries from monthly samples (July 2013 to August 2014) were used to identify microbes in seawater in four size fractions: >63 m (zooplankton and large particles), 63 to 5 m (particles), 5 to 1 m (small particles/dividing cells), and <1 m (free-living prokaryotes). Analyses of microbial community composition highlight the importance of the microhabitat (e.g., particle-associated versus free-living lifestyle) as communities cluster by size fraction, and the microhabitat explains more of the community variability than measured environmental parameters, including pH, particle concentration, projected daily insolation, nutrients, and temperature. While temperature is statistically associated with community changes in the <1-m and 5-to 1-m fractions, none of the measured bulk seawater environmental variables are statistically significant in the larger-particle-associated fractions. These results, combined with high particle-associated community variability, especially in the largest size fraction (i.e., >63 m), suggest that particle composition, including eukaryotes and their associated microbiomes, may be an important factor in selecting for specific particle-associated bacteria. IMPORTANCEBy comparing levels of particle-associated and free-living bacterial diversity at a coastal location over the course of 14 months, we show that bacteria associated with particles are generally more diverse and appear to be less responsive to commonly measured environmental variables than free-living bacteria. These diverse and highly variable particle-associated communities are likely driven by differences in particle substrates both within the water column at a single time point and due to seasonal changes over the course of the year.
Time series studies have shown that some bacterial taxa occur only at specific times of the year while others are ubiquitous in spite of seasonal shifts in environmental variables. Here, we ask if these ubiquitous clades are generalists that grow over a wide range of environmental conditions, or clusters of strain-level environmental specialists. To answer this question, vibrio strains isolated at a coastal time series were phylogenetically and physiologically characterized revealing three dominant strategies within the vibrio: mesophiles, psychrophiles and apparently generalist broad thermal range clades. Thermal performance curves from laboratory growth rate experiments help explain field observations of relative abundances: the mesophilic clade grows optimally at temperatures 16°C higher than the psychrophilic clade. Strains in the broad thermal range clade all have similar optimal growth temperatures but also exhibit temperature-related tradeoffs with faster growth rates for warm temperature strains and broader growth ranges for strains from cool temperatures. Moreover, the mechanisms of thermal adaptation apparently differ based on evolutionary time scales: shifts in the temperature of maximal growth occur between deeply branching clades but thermal performance curve shape changes on shorter time scales. Thus, apparently ubiquitous clades are likely not generalists, but contain subclusters with distinct environmental preferences.
Seaweed‐associated microbiota are essential for the health and resilience of nearshore ecosystems, marine biogeochemical cycling, and host health. Yet much remains unknown about the ecology of seaweed–microbe symbioses. In this study, we quantified fine‐scale patterns of microbial community structure across distinct anatomical regions of the kelp Laminaria setchellii. These anatomical regions represent a gradient of tissue ages: perennial holdfasts can be several years old, whereas stipe epicortex and blades are younger annual structures. Within blades, new growth occurs at the base, while the blade tips may be several months old and undergoing senescence. We hypothesized that microbial communities will differ across anatomical regions (holdfast, stipe, blade base, and blade tip), such that younger tissues will harbor fewer microbes that are more consistent across replicate individuals. Our data support this hypothesis, with the composition of bacterial (16S rRNA gene) and microeukaryote (18S rRNA gene) communities showing significant differences across the four anatomical regions, with the surfaces of older tissues (holdfast and blade tips) harboring significantly greater microbial richness compared to the younger tissues of the meristematic region. Additional samples collected from the surfaces of new L. setchellii recruits (<1y old) also showed differences in microbial community structure across anatomical regions, which demonstrates that these microbial differences are established early. We also observed this pattern in two additional algal species, suggesting that microbial community structure across host anatomy may be a common feature of the seaweed microbiome.
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