Consistent effects of independent domestication events on the plant microbiota.

The effect of plant domestication on plant-microbe interactions remains difficult to prove. In this study, we provide evidence of a domestication effect on the composition and abundance of the plant microbiota. We focused on the genus Phaseolus, which underwent four independent domestication events within two species (P. vulgaris and P. lunatus), providing multiple replicates of a process spanning thousands of years. We targeted Phaseolus seeds to identify a link between domesticated traits and bacterial community composition as Phaseolus seeds have been subject to large and consistent phenotypic changes during these independent domestication events. The seed bacterial communities of representative plant accessions from subpopulations descended from each domestication event were analyzed under controlled and field conditions. The results showed that independent domestication events led to similar seed bacterial community signatures in independently domesticated plant populations, which could be partially explained by selection for common domesticated plant phenotypes. Our results therefore provide evidence of a consistent effect of plant domestication on seed microbial community composition and abundance and offer avenues for applying knowledge of the impact of plant domestication on the plant microbiota to improve microbial applications in agriculture.

Gill-associated bacteria are homogeneously selected in amphibious mangrove crabs to sustain host intertidal adaptation.

BACKGROUND: The transition from water to air is a key event in the evolution of many marine organisms to access new food sources, escape water hypoxia, and exploit the higher and temperature-independent oxygen concentration of air. Despite the importance of microorganisms in host adaptation, their contribution to overcoming the challenges posed by the lifestyle changes from water to land is not well understood. To address this, we examined how microbial association with a key multifunctional organ, the gill, is involved in the intertidal adaptation of fiddler crabs, a dual-breathing organism. RESULTS: Electron microscopy revealed a rod-shaped bacterial layer tightly connected to the gill lamellae of the five crab species sampled across a latitudinal gradient from the central Red Sea to the southern Indian Ocean. The gill bacterial community diversity assessed with 16S rRNA gene amplicon sequencing was consistently low across crab species, and the same actinobacterial group, namely Ilumatobacter, was dominant regardless of the geographic location of the host. Using metagenomics and metatranscriptomics, we detected that these members of actinobacteria are potentially able to convert ammonia to amino acids and may help eliminate toxic sulphur compounds and carbon monoxide to which crabs are constantly exposed. CONCLUSIONS: These results indicate that bacteria selected on gills can play a role in the adaptation of animals in dynamic intertidal ecosystems. Hence, this relationship is likely to be important in the ecological and evolutionary processes of the transition from water to air and deserves further attention, including the ontogenetic onset of this association. Video Abstract.

The identification of the new species Nitratireductor thuwali sp. nov. reveals the untapped diversity of hydrocarbon-degrading culturable bacteria from the arid mangrove sediments of the Red Sea.

Introduction: The geological isolation, lack of freshwater inputs and specific internal water circulations make the Red Sea one of the most extreme-and unique-oceans on the planet. Its high temperature, salinity and oligotrophy, along with the consistent input of hydrocarbons due to its geology (e.g., deep-sea vents) and high oil tankers traffic, create the conditions that can drive and influence the assembly of unique marine (micro)biomes that evolved to cope with these multiple stressors. We hypothesize that mangrove sediments, as a model-specific marine environment of the Red Sea, act as microbial hotspots/reservoirs of such diversity not yet explored and described. Methods: To test our hypothesis, we combined oligotrophic media to mimic the Red Sea conditions and hydrocarbons as C-source (i.e., crude oil) with long incubation time to allow the cultivation of slow-growing environmentally (rare or uncommon) relevant bacteria. Results and discussion: This approach reveals the vast diversity of taxonomically novel microbial hydrocarbon degraders within a collection of a few hundred isolates. Among these isolates, we characterized a novel species, Nitratireductor thuwali sp. nov., namely, Nit1536T. It is an aerobic, heterotrophic, Gram-stain-negative bacterium with optimum growth at 37°C, 8 pH and 4% NaCl, whose genome and physiological analysis confirmed the adaptation to extreme and oligotrophic conditions of the Red Sea mangrove sediments. For instance, Nit1536T metabolizes different carbon substrates, including straight-chain alkanes and organic acids, and synthesizes compatible solutes to survive in salty mangrove sediments. Our results showed that the Red Sea represent a source of yet unknown novel hydrocarbon degraders adapted to extreme marine conditions, and their discovery and characterization deserve further effort to unlock their biotechnological potential.

The microbial landscape in bioturbated mangrove sediment: A resource for promoting nature-based solutions for mangroves.

Globally, soils and sediments are affected by the bioturbation activities of benthic species. The consequences of these activities are particularly impactful in intertidal sediment, which is generally anoxic and nutrient-poor. Mangrove intertidal sediments are of particular interest because, as the most productive forests and one of the most important stores of blue carbon, they provide global-scale ecosystem services. The mangrove sediment microbiome is fundamental for ecosystem functioning, influencing the efficiency of nutrient cycling and the abundance and distribution of key biological elements. Redox reactions in bioturbated sediment can be extremely complex, with one reaction creating a cascade effect on the succession of respiration pathways. This facilitates the overlap of different respiratory metabolisms important in the element cycles of the mangrove sediment, including carbon, nitrogen, sulphur and iron cycles, among others. Considering that all ecological functions and services provided by mangrove environments involve microorganisms, this work reviews the microbial roles in nutrient cycling in relation to bioturbation by animals and plants, the main mangrove ecosystem engineers. We highlight the diversity of bioturbating organisms and explore the diversity, dynamics and functions of the sediment microbiome, considering both the impacts of bioturbation. Finally, we review the growing evidence that bioturbation, through altering the sediment microbiome and environment, determining a 'halo effect', can ameliorate conditions for plant growth, highlighting the potential of the mangrove microbiome as a nature-based solution to sustain mangrove development and support the role of this ecosystem to deliver essential ecological services.

Enzyme adaptation to habitat thermal legacy shapes the thermal plasticity of marine microbiomes.

Microbial communities respond to temperature with physiological adaptation and compositional turnover. Whether thermal selection of enzymes explains marine microbiome plasticity in response to temperature remains unresolved. By quantifying the thermal behaviour of seven functionally-independent enzyme classes (esterase, extradiol dioxygenase, phosphatase, beta-galactosidase, nuclease, transaminase, and aldo-keto reductase) in native proteomes of marine sediment microbiomes from the Irish Sea to the southern Red Sea, we record a significant effect of the mean annual temperature (MAT) on enzyme response in all cases. Activity and stability profiles of 228 esterases and 5 extradiol dioxygenases from sediment and seawater across 70 locations worldwide validate this thermal pattern. Modelling the esterase phase transition temperature as a measure of structural flexibility confirms the observed relationship with MAT. Furthermore, when considering temperature variability in sites with non-significantly different MATs, the broadest range of enzyme thermal behaviour and the highest growth plasticity of the enriched heterotrophic bacteria occur in samples with the widest annual thermal variability. These results indicate that temperature-driven enzyme selection shapes microbiome thermal plasticity and that thermal variability finely tunes such processes and should be considered alongside MAT in forecasting microbial community thermal response.

Safeguarding Imperiled Biodiversity and Evolutionary Processes in the Wallacea Center of Endemism.

Wallacea-the meeting point between the Asian and Australian fauna-is one of the world's largest centers of endemism. Twenty-three million years of complex geological history have given rise to a living laboratory for the study of evolution and biodiversity, highly vulnerable to anthropogenic pressures. In the present article, we review the historic and contemporary processes shaping Wallacea's biodiversity and explore ways to conserve its unique ecosystems. Although remoteness has spared many Wallacean islands from the severe overexploitation that characterizes many tropical regions, industrial-scale expansion of agriculture, mining, aquaculture and fisheries is damaging terrestrial and aquatic ecosystems, denuding endemics from communities, and threatening a long-term legacy of impoverished human populations. An impending biodiversity catastrophe demands collaborative actions to improve community-based management, minimize environmental impacts, monitor threatened species, and reduce wildlife trade. Securing a positive future for Wallacea's imperiled ecosystems requires a fundamental shift away from managing marine and terrestrial realms independently.

Environmental micro-niche filtering shapes bacterial pioneer communities during primary colonization of a Himalayas' glacier forefield.

The pedogenesis from the mineral substrate released upon glacier melting has been explained with the succession of consortia of pioneer microorganisms, whose structure and functionality are determined by the environmental conditions developing in the moraine. However, the microbiome variability that can be expected in the environmentally heterogeneous niches occurring in a moraine at a given successional stage is poorly investigated. In a 50 m2 area in the forefield of the Lobuche glacier (Himalayas, 5050 m above sea level), we studied six sites of primary colonization presenting different topographical features (orientation, elevation and slope) and harbouring greyish/dark biological soil crusts (BSCs). The spatial vicinity of the sites opposed to their topographical differences, allowed us to examine the effect of environmental conditions independently from the time of deglaciation. The bacterial microbiome diversity and their co-occurrence network, the bacterial metabolisms predicted from 16S rRNA gene high-throughput sequencing, and the microbiome intact polar lipids were investigated in the BSCs and the underlying sediment deep layers (DLs). Different bacterial microbiomes inhabited the BSCs and the DLs, and their composition varied among sites, indicating a niche-specific role of the micro-environmental conditions in the bacterial communities' assembly. In the heterogeneous sediments of glacier moraines, physico-chemical and micro-climatic variations at the site-spatial scale are crucial in shaping the microbiome microvariability and structuring the pioneer bacterial communities during pedogenesis.

Bioturbation Intensity Modifies the Sediment Microbiome and Biochemistry and Supports Plant Growth in an Arid Mangrove System.

In intertidal systems, the type and role of interactions among sediment microorganisms, animals, plants and abiotic factors are complex and not well understood. Such interactions are known to promote nutrient provision and cycling, and their dynamics and relationships may be of particular importance in arid microtidal systems characterized by minimal nutrient input. Focusing on an arid mangrove ecosystem on the central Red Sea coast, we investigated the effect of crab bioturbation intensity (comparing natural and manipulated high levels of bioturbation intensity) on biogeochemistry and bacterial communities of mangrove sediments, and on growth performance of Avicennia marina, over a period of 16 months. Along with pronounced seasonal patterns with harsh summer conditions, in which high sediment salinity, sulfate and temperature, and absence of tidal flooding occur, sediment bacterial diversity and composition, sediment physicochemical conditions, and plant performance were significantly affected by crab bioturbation intensity. For instance, bioturbation intensity influenced components of nitrogen, carbon, and phosphate cycling, bacterial relative abundance (i.e., Bacteroidia, Proteobacteria and Rhodothermi) and their predicted functionality (i.e., chemoheterotrophy), likely resulting from enhanced metabolic activity of aerobic bacteria. The complex interactions among bacteria, animals, and sediment chemistry in this arid mangrove positively impact plant growth. We show that a comprehensive approach targeting multiple biological levels provides useful information on the ecological status of mangrove forests. IMPORTANCE Bioturbation is one of the most important processes that governs sediment biocenosis in intertidal systems. By facilitating oxygen penetration into anoxic layers, bioturbation alters the overall sediment biogeochemistry. Here, we investigate how high crab bioturbation intensity modifies the mangrove sediment bacterial community, which is the second largest component of mangrove sediment biomass and plays a significant role in major biogeochemical processes. We show that the increase in crab bioturbation intensity, by ameliorating the anoxic condition of mangrove sediment and promoting sediment bacterial diversity in favor of a beneficial bacterial microbiome, improves mangrove tree growth in arid environments. These findings have significant implications because they show how crabs, by farming the mangrove sediment, can enhance the overall capacity of the system to sustain mangrove growth, fighting climate change.

Approaching the domesticated plant holobiont from a community evolution perspective.

Plants establish a pivotal relationship with their microbiome and are often conceptualized as holobionts. Nonetheless, holobiont theories have attracted much criticism, especially concerning the fact that the holobiont is rarely a unit of selection. In previous work, we discussed how the plant microbiome can be considered to be an 'ecosystem on a leash', which is subject to the influence of natural selection acting on plant traits. We proposed that in domesticated plants the assembly of the plant microbiome can usefully be conceptualized as being subject to a 'double leash', which encompasses both the effect of artificial selection imposed by the domesticator on plant traits and the leash from the plant to the microbiome. Here we approach the domesticated plant holobiont, simply defined as a community of organisms, from a community evolution point of view, and show how community heritability (a measure of community selection) complements the 'double-leash' framework in providing a community-level view of plant domestication and its impact on plant-microbe interactions. We also propose simple experiments that could be performed to investigate whether plant domestication has altered the potential for community selection at the holobiont level.

Rootstock-scion combination contributes to shape diversity and composition of microbial communities associated with grapevine root system.

To alleviate biotic and abiotic stresses and enhance fruit yield, many crops are cultivated in the form of grafted plants, in which the shoot (scion) and root (rootstock) systems of different species are joined together. Because (i) the plant species determines the microbial recruitment from the soil to the root and (ii) both scion and rootstock impact the physiology, morphology and biochemistry of the grafted plant, it can be expected that their different combinations should affect the recruitment and assembly of plant microbiome. To test our hypothesis, we investigated at a field scale the bacterial and fungal communities associated with the root system of seven grapevine rootstock-scion combinations cultivated across 10 different vineyards. Following the soil type, which resulted in the main determinant of the grapevine root microbial community diversity, the rootstock-scion combination resulted more important than the two components taken alone. Notably, the microbiome differences among the rootstock-scion combinations were mainly dictated by the changes in the relative abundance of microbiome members rather than by their presence/absence. These results reveal that the microbiome of grafted grapevine root systems is largely influenced by the combination of rootstock and scion, which affects the microbial diversity uptaken from soil.

Rhizosheath-root system changes exopolysaccharide content but stabilizes bacterial community across contrasting seasons in a desert environment.

BACKGROUND: In hot deserts daily/seasonal fluctuations pose great challenges to the resident organisms. However, these extreme ecosystems host unique microenvironments, such as the rhizosheath-root system of desert speargrasses in which biological activities and interactions are facilitated by milder conditions and reduced fluctuations. Here, we examined the bacterial microbiota associated with this structure and its surrounding sand in the desert speargrass Stipagrostis pungens under the contrasting environmental conditions of summer and winter in the Sahara Desert. RESULTS: The belowground rhizosheath-root system has higher nutrient and humidity contents, and cooler temperatures than the surrounding sand. The plant responds to the harsh environmental conditions of the summer by increasing the abundance and diversity of extracellular polymeric substances (EPS) compared to the winter. On the contrary, the bacterial community associated with the rhizosheath-root system and its interactome remain stable and, unlike the bulk sand, are unaffected by the seasonal environmental variations. The rhizosheath-root system bacterial communities are consistently dominated by Actinobacteria and Alphaproteobacteria and form distinct bacteria communities from those of bulk sand in the two seasons. The microbiome-stabilization mediated by the plant host acts to consistently retain beneficial bacteria with multiple plant growth promoting functions, including those capable to produce EPS, which increase the sand water holding capacity ameliorating the rhizosheath micro-environment. CONCLUSIONS: Our results reveal the capability of plants in desert ecosystems to stabilize their below ground microbial community under seasonal contrasting environmental conditions, minimizing the heterogeneity of the surrounding bulk sand and contributing to the overall holobiont resilience under poly-extreme conditions.

Morphological characteristics and abundance of prokaryotes associated with gills in mangrove brachyuran crabs living along a tidal gradient.

Due to the chemico-physical differences between air and water, the transition from aquatic life to the land poses several challenges for animal evolution, necessitating morphological, physiological and behavioural adaptations. Microbial symbiosis is known to have played an important role in eukaryote evolution, favouring host adaptation under changing environmental conditions. We selected mangrove brachyuran crabs as a model group to investigate the prokaryotes associated with the gill of crabs dwelling at different tidal levels (subtidal, intertidal and supratidal). In these animals, the gill undergoes a high selective pressure, finely regulating multiple physiological functions during both animal submersion under and emersion from the periodical tidal events. We hypothesize that similarly to other marine animals, the gills of tidal crabs are consistently colonized by prokaryotes that may quantitatively change along the environmental gradient driven by the tides. Using electron microscopy techniques, we found a thick layer of prokaryotes over the gill surfaces of all of 12 crab species from the mangrove forests of Saudi Arabia, Kenya and South Africa. We consistently observed two distinct morphotypes (rod- and spherical-shaped), positioned horizontally and/or perpendicularly to the gill surface. The presence of replicating cells indicated that the prokaryote layer is actively growing on the gill surface. Quantitative analysis of scanning electron microscopy images and the quantification of the bacterial 16S rRNA gene by qPCR revealed a higher specific abundance of prokaryote cells per gill surface area in the subtidal species than those living in the supratidal zone. Our results revealed a correlation between prokaryote colonization of the gill surfaces and the host lifestyle. This finding indicates a possible role of prokaryote partnership within the crab gills, with potential effects on animal adaptation to different levels of the intertidal gradient present in the mangrove ecosystem.

Destabilization of the Bacterial Interactome Identifies Nutrient Restriction-Induced Dysbiosis in Insect Guts.

Stress-associated dysbiosis of microbiome can have several configurations that, under an energy landscape conceptual framework, can change from one configuration to another due to different alternating selective forces. It has been proposed-according to the Anna Karenina Principle-that in stressed individuals the microbiome are more dispersed (i.e., with a higher within-beta diversity), evidencing the grade of dispersion as indicator of microbiome dysbiosis. We hypothesize that although dysbiosis leads to different microbial communities in terms of beta diversity, these are not necessarily differently dispersed (within-beta diversity), but they form disrupted networks that make them less resilient to stress. To test our hypothesis, we select nutrient restriction (NR) stress that impairs host fitness but does not introduce overt microbiome selectors, such as toxic compounds and pathogens. We fed the polyphagous black soldier fly, Hermetia illucens, with two NR diets and a control full-nutrient (FN) diet. NR diets were dysbiotic because they strongly affected insect growth and development, inducing significant microscale changes in physiochemical conditions of the gut compartments. NR diets established new configurations of the gut microbiome compared to FN-fed guts but with similar dispersion. However, these new configurations driven by the deterministic changes induced by NR diets were reflected in rarefied, less structured, and less connected bacterial interactomes. These results suggested that while the dispersion cannot be considered a consistent indicator of the unhealthy state of dysbiotic microbiomes, the capacity of the community members to maintain network connections and stability can be an indicator of the microbial dysbiotic conditions and their incapacity to sustain the holobiont resilience and host homeostasis. IMPORTANCE Changes in diet play a role in reshaping the gut microbiome in animals, inducing dysbiotic configurations of the associated microbiome. Although studies have reported on the effects of specific nutrient contents on the diet, studies regarding the conditions altering the microbiome configurations and networking in response to diet changes are limited. Our results showed that nutrient poor diets determine dysbiotic states of the host with reduction of insect weight and size, and increase of the times for developmental stage. Moreover, the poor nutrient diets lead to changes in the compositional diversity and network interaction properties of the gut microbial communities. Our study adds a new component to the understanding of the ecological processes associated with dysbiosis, by disentangling consequences of diets on microbiome dysbiosis that is manifested with the disruption of microbiome networking properties rather than changes in microbiome dispersion and beta diversity.

The plant rhizosheath-root niche is an edaphic "mini-oasis" in hyperarid deserts with enhanced microbial competition.

Plants have evolved unique morphological and developmental adaptations to cope with the abiotic stresses imposed by (hyper)arid environments. Such adaptations include the formation of rhizosheath-root system in which mutualistic plant-soil microbiome associations are established: the plant provides a nutrient-rich and shielded environment to microorganisms, which in return improve plant-fitness through plant growth promoting services. We hypothesized that the rhizosheath-root systems represent refuge niches and resource islands for the desert edaphic microbial communities. As a corollary, we posited that microorganisms compete intensively to colonize such "oasis" and only those beneficial microorganisms improving host fitness are preferentially selected by plant. Our results show that the belowground rhizosheath-root micro-environment is largely more hospitable than the surrounding gravel plain soil with higher nutrient and humidity contents, and cooler temperatures. By combining metabarcoding and shotgun metagenomics, we demonstrated that edaphic microbial biomass and community stability increased from the non-vegetated soils to the rhizosheath-root system. Concomitantly, non-vegetated soil communities favored autotrophy lifestyle while those associated with the plant niches were mainly heterotrophs and enriched in microbial plant growth promoting capacities. An intense inter-taxon microbial competition is involved in the colonization and homeostasis of the rhizosheath zone, as documented by significant enrichment of antibiotic resistance genes and CRISPR-Cas motifs. Altogether, our results demonstrate that rhizosheath-root systems are "edaphic mini-oases" and microbial diversity hotspots in hyperarid deserts. However, to colonize such refuge niches, the desert soil microorganisms compete intensively and are therefore prepared to outcompete potential rivals.

Aridity modulates belowground bacterial community dynamics in olive tree.

Aridity negatively affects the diversity and abundance of edaphic microbial communities and their multiple ecosystem services, ultimately impacting vegetation productivity and biotic interactions. Investigation about how plant-associated microbial communities respond to increasing aridity is of particular importance, especially in light of the global climate change predictions. To assess the effect of aridity on plant associated bacterial communities, we investigated the diversity and co-occurrence of bacteria associated with the bulk soil and the root system of olive trees cultivated in orchards located in higher, middle and lower arid regions of Tunisia. The results indicated that the selective process mediated by the plant root system is amplified with the increment of aridity, defining distinct bacterial communities, dominated by aridity-winner and aridity-loser bacteria negatively and positively correlated with increasing annual rainfall, respectively. Aridity regulated also the co-occurrence interactions among bacteria by determining specific modules enriched with one of the two categories (aridity-winners or aridity-losers), which included bacteria with multiple PGP functions against aridity. Our findings provide new insights into the process of bacterial assembly and interactions with the host plant in response to aridity, contributing to understand how the increasing aridity predicted by climate changes may affect the resilience of the plant holobiont.

The effect of plant domestication on host control of the microbiota.

Macroorganisms are colonized by microbial communities that exert important biological and ecological functions, the composition of which is subject to host control and has therefore been described as "an ecosystem on a leash". However, domesticated organisms such as crop plants are subject to both artificial selection and natural selection exerted by the agricultural ecosystem. Here, we propose a framework for understanding how host control of the microbiota is influenced by domestication, in which a double leash acts from domesticator to host and host to microbes. We discuss how this framework applies to a plant compartment that has demonstrated remarkable phenotypic changes during domestication: the seed.

A functional analysis reveals extremely low redundancy in global mangrove invertebrate fauna.

Deforestation results in habitat fragmentation, decreasing diversity, and functional degradation. For mangroves, no data are available on the impact of deforestation on the diversity and functionality of the specialized invertebrate fauna, critical for their functioning. We compiled a global dataset of mangrove invertebrate fauna comprising 364 species from 16 locations, classified into 64 functional entities (FEs). For each location, we calculated taxonomic distinctness (Δ+), functional richness (FRi), functional redundancy (FRe), and functional vulnerability (FVu) to assess functional integrity. Δ+ and FRi were significantly related to air temperature but not to geomorphic characteristics, mirroring the global biodiversity anomaly of mangrove trees. Neither of those two indices was linked to forest area, but both sharply decreased in human-impacted mangroves. About 60% of the locations showed an average FRe < 2, indicating that most of the FEs comprised one species only. Notable exceptions were the Eastern Indian Ocean and west Pacific Ocean locations, but also in this region, 57% of the FEs had no redundancy, placing mangroves among the most vulnerable ecosystems on the planet. Our study shows that despite low redundancy, even small mangrove patches host truly multifunctional faunal assemblages, ultimately underpinning their services. However, our analyses also suggest that even a modest local loss of invertebrate diversity could have significant negative consequences for many mangroves and cascading effects for adjacent ecosystems. This pattern of faunal-mediated ecosystem functionality is crucial for assessing the vulnerability of mangrove forests to anthropogenic impact and provides an approach to planning their effective conservation and restoration.

Compartmentalization of bacterial and fungal microbiomes in the gut of adult honeybees.

The core gut microbiome of adult honeybee comprises a set of recurring bacterial phylotypes, accompanied by lineage-specific, variable, and less abundant environmental bacterial phylotypes. Several mutual interactions and functional services to the host, including the support provided for growth, hormonal signaling, and behavior, are attributed to the core and lineage-specific taxa. By contrast, the diversity and distribution of the minor environmental phylotypes and fungal members in the gut remain overlooked. In the present study, we hypothesized that the microbial components of forager honeybees (i.e., core bacteria, minor environmental phylotypes, and fungal members) are compartmentalized along the gut portions. The diversity and distribution of such three microbial components were investigated in the context of the physico-chemical conditions of different gut compartments. We observed that changes in the distribution and abundance of microbial components in the gut are consistently compartment-specific for all the three microbial components, indicating that the ecological and physiological interactions among the host and microbiome vary with changing physico-chemical and metabolic conditions of the gut.