Multidimensional specialization and generalization are pervasive in soil prokaryotes

Hernández, Damián; Kiesewetter, Kasey N.; Almeida, Brianna K.; Revillini, Daniel; Afkhami, Michelle E.

doi:10.1038/s41559-023-02149-y

Cited by 6 publications

(6 citation statements)

References 70 publications

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“…A new ecological concept posits that all microbes evolve in a particular niche that shapes their microbiome, with microbes adopting either multidimensional specialization or multidimensional generalization ( Hernandez et al, 2023 ). From the present lab-based study, it can be concluded that the stringent and narrow parameters of various intertidal estuarine mangrove niches drove the multidimensional specialization of the heterotrophic diazotroph communities.…”

Section: Discussionmentioning

confidence: 99%

“…From the present lab-based study, it can be concluded that the stringent and narrow parameters of various intertidal estuarine mangrove niches drove the multidimensional specialization of the heterotrophic diazotroph communities. Multidimensional specialists face more environmental constraints during their evolution and are less resilient and less common compared to their generalist counterparts ( Hernandez et al, 2023 ). The extreme nature of the estuarine mangrove-related rhizospheric sediment parameters (related to pH, salinity, temperature, soil texture, dynamic relative abundances of bacterial taxa, deficiencies in N, P, and Fe, presence of sulfides, and anoxicity) structured the heterotrophic diazotroph communities, which exhibited diverse metabolic functions that aid BNF.…”

Section: Discussionmentioning

confidence: 99%

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Estuarine mangrove niches select cultivable heterotrophic diazotrophs with diverse metabolic potentials—a prospective cross-dialog for functional diazotrophy

Mondal,

Biswas,

Chowdhury

et al. 2024

Front. Microbiol.

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IntroductionBiological nitrogen fixation (BNF), an unparalleled metabolic novelty among living microorganisms on earth, globally contributes ~88-101 Tg N year−1 to natural ecosystems, ~56% sourced from symbiotic BNF while ~22-45% derived from free-living nitrogen fixers (FLNF). The success of symbiotic BNF is largely dependent on its interaction with host-plant, however ubiquitous environmental heterotrophic FLNFs face many limitations in their immediate ecological niches to sustain unhindered BNF. The autotrophic FLNFs like cyanobacteria and oceanic heterotrophic diazotrophs have been well studied about their contrivances acclimated/adapted by these organisms to outwit the environmental constraints for functional diazotrophy. However, FLNF heterotrophs face more adversity in executing BNF under stressful estuarine/marine/aquatic habitats.MethodsIn this study a large-scale cultivation-dependent investigation was accomplished with 190 NCBI accessioned and 45 non-accessioned heterotrophic FLNF cultivable bacterial isolates (total 235) from halophilic estuarine intertidal mangrove niches of Indian Sundarbans, a Ramsar site and UNESCO proclaimed World Heritage Site. Assuming ~1% culturability of the microbial community, the respective niches were also studied for representing actual bacterial diversity via cultivation-independent next-generation sequencing of V3-V4 rRNA regions.ResultsBoth the studies revealed a higher abundance of culturable Gammaproteobacteria followed by Firmicutes, the majority of 235 FLNFs studied belonging to these two classes. The FLNFs displayed comparable selection potential in media for free nitrogen fixers and iron-oxidizing bacteria, linking diazotrophy with iron oxidation, siderophore production, phosphorus solubilization, phosphorus uptake and accumulation as well as denitrification.DiscussionThis observation validated the hypothesis that under extreme estuarine mangrove niches, diazotrophs are naturally selected as a specialized multidimensional entity, to expedite BNF and survive. Earlier metagenome data from mangrove niches demonstrated a microbial metabolic coupling among C, N, P, S, and Fe cycling in mangrove sediments, as an adaptive trait, evident with the co-abundant respective functional genes, which corroborates our findings in cultivation mode for multiple interrelated metabolic potential facilitating BNF in a challenging intertidal mangrove environment.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Estuarine mangrove niches select cultivable heterotrophic diazotrophs with diverse metabolic potentials—a prospective cross-dialog for functional diazotrophy

Mondal,

Biswas,

Chowdhury

et al. 2024

Front. Microbiol.

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“…We hypothesized that estimates of differentiation are similar between individual axes corresponding to the same niche type, while there may be differences between types and in relation to the full niche. Empirical studies of macro-organisms (reviewed by Carscadden et al, 2020) and microorganisms (Hernandez et al, 2023), including fungi (Chaloner et al, 2020;Maynard et al, 2019), have yielded mixed results about how much niche differentiation along one axis reflects differentiation along others. In general, we found that niche differentiation with respect to a niche type was consistently moderately correlated with differentiation along the component single niche axes within the type, though there was notably more variation among the axes in AR type.…”

Section: Discussionmentioning

confidence: 99%

“…However, this approach has received criticism because of the weak or untested linkage between trait space and niche space (Blonder et al, 2018). An alternative approach is to describe niches based on organism distributions along gradients; for example, soil prokaryote niches have been estimated on the basis of distribution and abundance in soils with widely varying abiotic characteristics throughout the United States (Hernandez et al, 2023). Although popular, this approach has to overcome the confounding effect of dispersal limitation (Araújo & Guisan, 2006;Broennimann et al, 2012;Kambach et al, 2019), and typically provides no indication about mechanisms in the interaction milieu that contribute to the realized niche (McGill et al, 2006).…”

Section: Introductionmentioning

confidence: 99%

Niche types and community assembly

Davison,

Gerz,

Hiiesalu

et al. 2023

Ecology Letters

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Studies of niche differentiation and biodiversity often focus on a few niche dimensions due to the methodological challenge of describing hyperdimensional niche space. However, this may limit our understanding of community assembly processes. We used the full spectrum of realized niche types to study arbuscular mycorrhizal fungal communities: distinguishing abiotic and biotic, and condition and resource, axes. Estimates of differentiation in relation to different niche types were only moderately correlated. However, coexisting taxon niches were consistently less differentiated than expected, based on a regional null model, indicating the importance of habitat filtering at that scale. Nonetheless, resource niches were relatively more differentiated than condition niches, which is consistent with the effect of a resource niche‐based coexistence mechanism. Considering niche types, and in particular distinguishing resource and condition niches, provides a more complete understanding of community assembly, compared with studying individual niche axes or the full niche.

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“…To calculate niche breadth for ASVs, we first eliminated ASVs only found at one site (1878 ASVs reduced to 832 ASVs), equivalent to a 5% sample occupancy cutoff (stricter than (13,59) but not as conservative as (113)). Next, we used the R package MicroNiche v1.0.0 (42), with the default settings for the limit of quantification (LOQ) threshold (q = 1.6).…”

Section: Community Assembly Analysismentioning

confidence: 99%

Antarctic geothermal soils exhibit an absence of regional habitat generalist microorganisms

Noell,

Abbaszadeh,

Richards

et al. 2024

Preprint

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Active geothermal systems are relatively rare in Antarctica and represent metaphorical islands ideal to test microbial dispersal. In this study, we tested the macroecological concept that high dispersal rates result in communities being dominated by either habitat generalists or specialists by investigating the microbial communities on four geographically separated geothermal sites on three Antarctic volcanoes (Mts. Erebus, Melbourne and Rittman). We found that the microbial communities at higher temperature sites (Tramway Ridge on Erebus and Rittmann) were unique from each other and were dominated by a variety of novelArchaeafrom classNitrososphaeria, while lower temperature sites (Western Crater on Erebus and Melbourne) had characteristically mesophilic communities (Planctomycetes, Acidobacteriota,etc) that were highly similar. We found that 97% of the detected microbial taxa were regional habitat specialists, with no generalists, with community assembly driven by high dispersal rates and drift (25 and 30% of community assembly, respectively), not environmental selection.

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Multidimensional specialization and generalization are pervasive in soil prokaryotes

Cited by 6 publications

References 70 publications

Estuarine mangrove niches select cultivable heterotrophic diazotrophs with diverse metabolic potentials—a prospective cross-dialog for functional diazotrophy

Estuarine mangrove niches select cultivable heterotrophic diazotrophs with diverse metabolic potentials—a prospective cross-dialog for functional diazotrophy

Niche types and community assembly

Antarctic geothermal soils exhibit an absence of regional habitat generalist microorganisms

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