RESUMEN
Seaweeds play a strong ecological and economical role along the world's coastlines, where they support industries (e.g., aquaculture, bioproducts) and essential ecosystem services (e.g., biodiversity, fisheries, carbon capture). Evidence from wild and cultured seaweeds suggests that microorganisms play crucial roles in their health and functioning, prompting the need for considering seaweeds and their microbiome as a coherent entity or "holobiont." Here we show that the number of studies investigating seaweed hosts and their microbiome have increased in the last two decades. This likely reflects the increase in the appreciation of the importance of microbiomes for eukaryotic hosts, improved molecular approaches used to characterize their interactions, and increasing interest in commercial use of seaweeds. However, although increasing, most studies of seaweed holobionts have focused on (i) a few seaweed species of ecological or commercial significance, (ii) interactions involving only bacteria, and (iii) descriptive rather than experimental approaches. The relatively few experimental studies have mostly focused on manipulating abiotic factors to examine responses of seaweeds and their microbiome. Of the few studies that directly manipulated microorganisms to investigate their effects on seaweeds, most were done in laboratory or aquaria. We emphasize the need to move beyond the descriptions of patterns to experimental approaches for understanding causation and mechanisms. We argue that such experimental approaches are necessary for a better understanding of seaweed holobionts, for management actions for wild and cultivated seaweeds, and to better integrate studies of seaweed holobionts with the broader fields of seaweed ecology and biology, which are strongly experimental.
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Microbiota , Algas Marinas , SimbiosisRESUMEN
Host-associated microbiota are critical for eukaryotic host functioning, to the extent that hosts and their associated microbial communities are often considered "holobionts". Most studies of holobionts have focused on descriptive approaches or have used model systems, usually in the laboratory, to understand host-microbiome interactions. To advance our understanding of host-microbiota interactions and their wider ecological impacts, we need experimental frameworks that can explore causation in non-model hosts, which often have highly diverse microbiota, and in their natural ecological setting (i.e. in the field). We used a dominant habitat-forming seaweed, Hormosira banksii, to explore these issues and to experimentally test host-microbiota interactions in a non-model holobiont. The experimental protocols were aimed at trying to disentangle microbially mediated effects on hosts from direct effects on hosts associated with the methods employed to manipulate host-microbiota. This was done by disrupting the microbiome, either through removal/disruption using a combination of antimicrobial treatments, or additions of specific taxa via inoculations, or a combination of thew two. The experiments were done in mesocosms and in the field. Three different antibiotic treatments were used to disrupt seaweed-associated microbiota to test whether disturbances of microbiota, particularly bacteria, would negatively affect host performance. Responses of bacteria to these disturbances were complex and differed substantially among treatments, with some antibacterial treatments having little discernible effect. However, the temporal sequence of responses antibiotic treatments, changes in bacterial diversity and subsequent decreases in host performance, strongly suggested an effect of the microbiota on host performance in some treatments, as opposed to direct effects of the antibiotics. To further test these effects, we used 16S-rRNA-gene sequencing to identify bacterial taxa that were either correlated, or uncorrelated, with poor host performance following antibiotic treatment. These were then isolated and used in inoculation experiments, independently or in combination with the previously used antibiotic treatments. Negative effects on host performance were strongest where specific microbial antimicrobials treatments were combined with inoculations of strains that were correlated with poor host performance. For these treatments, negative host effects persisted the entire experimental period (12 days), even though treatments were only applied at the beginning of the experiment. Host performance recovered in all other treatments. These experiments provide a framework for exploring causation and disentangling microbially mediated vs. direct effects on hosts for ecologically important, non-model holobionts in the field. This should allow for better predictions of how these systems will respond to, and potentially mitigate, environmental disturbances in their natural context.
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Microbiota , Microbiota/fisiología , Bacterias/genética , Interacciones Microbiota-Huesped , AntibacterianosRESUMEN
Habitat complexity is widely considered an important determinant of biodiversity, and enhancing complexity can play a key role in restoring degraded habitats. However, the effects of habitat complexity on ecosystem functioning - as opposed to biodiversity and community structure - are relatively poorly understood for artificial habitats, which dominate many coastlines. With Greening of Grey Infrastructure (GGI) approaches, or eco-engineering, increasingly being applied around the globe, it is important to understand the effects that modifying habitat complexity has on both biodiversity and ecological functioning in these highly modified habitats. We assessed how manipulating physical (primary substrate) and/or biogenic habitat (bivalves) complexity on intertidal artificial substrata affected filtration rates, net and gross primary productivity (NPP and GPP, respectively) and community respiration (CR) - as well as abundance of filter feeders and macro-algae and habitat use by cryptobenthic fish across six locations in three continents. We manipulated both physical and biogenic complexity using 1) flat or ridged (2.5 cm or 5 cm) settlement tiles that were either 2) unseeded or seeded with oysters or mussels. Across all locations, increasing physical and biogenic complexity (5 cm seeded tiles) had a significant effect on most ecological functioning variables, increasing overall filtration rates and community respiration of the assemblages on tiles but decreasing productivity (both GPP and NPP) across all locations. There were no overall effects of increasing either type of habitat complexity on cryptobenthic fish MaxN, total time in frame or macro-algal cover. Within each location, there were marked differences in the effects of habitat complexity. In Hobart, we found higher filtration, filter feeder biomass and community respiration on 5 cm tiles compared to flat tiles. However, at this location, both macro-algae cover and GPP decreased with increasing physical complexity. Similarly in Dublin, filtration, filter feeder biomass and community respiration were higher on 5 cm tiles compared to less complex tiles. In Sydney, filtration and filter feeder biomass were higher on seeded than unseeded tiles, and fish MaxN was higher on 5 cm tiles compared to flat tiles. On unseeded tiles in Sydney, filter feeder biomass also increased with increasing physical complexity. Our findings suggest that GGI solutions via increased habitat complexity are likely to have trade-offs among potentially desired functions, such as productivity and filtration rates, and variable effects on cryptobenthic fish communities. Importantly, our results show that the effects of GGI practices can vary markedly according to the environmental context and therefore should not be blindly and uniformly applied across the globe.
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Ecosistema , Ostreidae , Animales , Biodiversidad , Biomasa , PecesRESUMEN
The range-expansion of tropical herbivores due to ocean warming can profoundly alter temperate reef communities by overgrazing the seaweed forests that underpin them. Such ecological interactions may be mediated by changes to seaweed-associated microbiota in response to warming, but empirical evidence demonstrating this is rare. We experimentally simulated ocean warming and marine heatwaves (MHWs) to quantify effects on two dominant temperate seaweed species and their microbiota, as well as grazing by a tropical herbivore. The kelp Ecklonia radiata's microbiota in sustained warming and MHW treatments was enriched with microorganisms associated with seaweed disease and tissue degradation. In contrast, the fucoid Sargassum linearifolium's microbiota was unaffected by temperature. Consumption by the tropical sea-urchin Tripneustes gratilla was greater on Ecklonia where the microbiota had been altered by higher temperatures, while Sargassum's consumption was unaffected. Elemental traits (carbon, nitrogen), chemical defences (phenolics) and tissue bleaching of both seaweeds were generally unaffected by temperature. Effects of warming and MHWs on seaweed holobionts (host plus its microbiota) are likely species-specific. The effect of increased temperature on Ecklonia's microbiota and subsequent increased consumption suggest that changes to kelp microbiota may underpin kelp-herbivore interactions, providing novel insights into potential mechanisms driving change in species' interactions in warming oceans.
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Kelp , Microbiota , Algas Marinas , Kelp/fisiología , Ecosistema , Cambio Climático , Océanos y MaresRESUMEN
A fundamental question in holobiont biology is the extent to which microbiomes are determined by host characteristics regulated by their genotype. Studies on the interactions of host genotype and microbiomes are emerging but disentangling the role that host genotype has in shaping microbiomes remains challenging in natural settings. Host genotypes tend to be segregated in space and affected by different environments. Here we overcome this challenge by studying an unusual situation where host asexual (5 clonal lineages) and sexual genotypes (15 non-clonal lineages) of the same species co-occur under the same environment. This allowed us to partition the influence of morphological traits and genotype in shaping host-associated bacterial communities. Lamina-associated bacteria of co-occurring kelp sexual non-clonal (Ecklonia radiata) and asexual clonal (E. brevipes) morphs were compared to test whether host genotype influences microbiomes beyond morphology. Similarity of bacterial composition and predicted functions were evaluated among individuals within a single clonal genotype or among non-clonal genotypes of each morph. Higher similarity in bacterial composition and inferred functions were found among identical clones of E. brevipes compared to other clonal genotypes or unique non-clonal E. radiata genotypes. Additionally, bacterial diversity and composition differed significantly between the two morphs and were related with one morphological trait in E. brevipes (haptera). Thus, factors regulated by the host genotype (e.g. secondary metabolite production) likely drive differences in microbial communities between morphs. The strong association of genotype and microbiome found here highlights the importance of genetic relatedness of hosts in determining variability in their bacterial symbionts.
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Kelp , Microbiota , Humanos , Kelp/genética , Microbiota/genética , GenotipoRESUMEN
While marine kelp forests have provided valuable ecosystem services for millennia, the global ecological and economic value of those services is largely unresolved. Kelp forests are diminishing in many regions worldwide, and efforts to manage these ecosystems are hindered without accurate estimates of the value of the services that kelp forests provide to human societies. Here, we present a global estimate of the ecological and economic potential of three key ecosystem services - fisheries production, nutrient cycling, and carbon removal provided by six major forest forming kelp genera (Ecklonia, Laminaria, Lessonia, Macrocystis, Nereocystis, and Saccharina). Each of these genera creates a potential value of between $64,400 and $147,100/hectare each year. Collectively, they generate between $465 and $562 billion/year worldwide, with an average of $500 billion. These values are primarily driven by fisheries production (mean $29,900, 904 Kg/Ha/year) and nitrogen removal ($73,800, 657 Kg N/Ha/year), though kelp forests are also estimated to sequester 4.91 megatons of carbon from the atmosphere/year highlighting their potential as blue carbon systems for climate change mitigation. These findings highlight the ecological and economic value of kelp forests to society and will facilitate better informed marine management and conservation decisions.
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Ecosistema , Kelp , Humanos , Bosques , Cambio Climático , CarbonoRESUMEN
Bacterioplankton communities govern marine productivity and biogeochemical cycling, yet drivers of bacterioplankton assembly remain unclear. Here, we contrast the relative contribution of deterministic processes (environmental factors and biotic interactions) in driving temporal dynamics of bacterioplankton diversity at three different oceanographic time series locations, spanning 15° of latitude, which are each characterized by different environmental conditions and varying degrees of seasonality. Monthly surface samples (5.5 years) were analysed using 16S rRNA amplicon sequencing. The high- and mid-latitude sites of Maria Island and Port Hacking were characterized by high and intermediate levels of environmental heterogeneity, respectively, with both alpha diversity (72%; 24% of total variation) and beta diversity (32%; 30%) patterns within bacterioplankton assemblages explained by day length, ammonium, and mixed layer depth. In contrast, North Stradbroke Island, a sub-tropical location where environmental conditions are less variable, interspecific interactions were of increased importance in structuring bacterioplankton diversity (alpha: 33%; beta: 26%) with environment only contributing 11% and 13% to predicting diversity, respectively. Our results demonstrate that bacterioplankton diversity is the result of both deterministic environmental and biotic processes and that the importance of these different deterministic processes varies, potential in response to environmental heterogeneity.
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Organismos Acuáticos , Ecosistema , ARN Ribosómico 16S/genética , Plancton/genéticaRESUMEN
Antarctic sea-ice forms a complex and dynamic system that drives many ecological processes in the Southern Ocean. Sea-ice microalgae and their associated microbial communities are understood to influence nutrient flow and allocation in marine polar environments. Sea-ice microalgae and their microbiota can have high seasonal and regional (>1000 km2) compositional and abundance variation, driven by factors modulating their growth, symbiotic interactions and function. In contrast, our knowledge of small-scale variation in these communities is limited. Understanding variation across multiple scales and its potential drivers is critical for informing on how multiple stressors impact sea-ice communities and the functions they provide. Here, we characterized bacterial communities associated with sea-ice microalgae and the potential drivers that influence their variation across a range of spatial scales (metres to >10 kms) in a previously understudied area in Commonwealth Bay, East Antarctica where anomalous events have substantially and rapidly expanded local sea-ice coverage. We found a higher abundance and different composition of bacterial communities living in sea-ice microalgae closer to the shore compared to those further from the coast. Variation in community structure increased linearly with distance between samples. Ice thickness and depth to the seabed were found to be poor predictors of these communities. Further research on the small-scale environmental drivers influencing these communities is needed to fully understand how large-scale regional events can affect local function and ecosystem processes.
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Microalgas , Microbiota , Regiones Antárticas , Bahías , Ecosistema , Cubierta de HieloRESUMEN
Kelp forest ecosystems and their associated ecosystem services are declining around the world. In response, marine managers are working to restore and counteract these declines. Kelp restoration first started in the 1700s in Japan and since then has spread across the globe. Restoration efforts, however, have been largely disconnected, with varying methodologies trialled by different actors in different countries. Moreover, a small subset of these efforts are 'afforestation', which focuses on creating new kelp habitat, as opposed to restoring kelp where it previously existed. To distil lessons learned over the last 300 years of kelp restoration, we review the history of kelp restoration (including afforestation) around the world and synthesise the results of 259 documented restoration attempts spanning from 1957 to 2020, across 16 countries, five languages, and multiple user groups. Our results show that kelp restoration projects have increased in frequency, have employed 10 different methodologies and targeted 17 different kelp genera. Of these projects, the majority have been led by academics (62%), have been conducted at sizes of less than 1 ha (80%) and took place over time spans of less than 2 years. We show that projects are most successful when they are located near existing kelp forests. Further, disturbance events such as sea-urchin grazing are identified as regular causes of project failure. Costs for restoration are historically high, averaging hundreds of thousands of dollars per hectare, therefore we explore avenues to reduce these costs and suggest financial and legal pathways for scaling up future restoration efforts. One key suggestion is the creation of a living database which serves as a platform for recording restoration projects, showcasing and/or re-analysing existing data, and providing updated information. Our work establishes the groundwork to provide adaptive and relevant recommendations on best practices for kelp restoration projects today and into the future.
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Ecosistema , Restauración y Remediación Ambiental , Kelp , Animales , Cadena Alimentaria , Kelp/fisiología , Erizos de Mar/fisiologíaRESUMEN
Interactions between hosts and their microbiota are vital to the functioning and resilience of macro-organisms. Critically, for hosts that play foundational roles in communities, understanding what drives host-microbiota interactions is essential for informing ecosystem restoration and conservation. We investigated the relative influence of host traits and the surrounding environment on microbial communities associated with the foundational seaweed Phyllospora comosa. We quantified 16 morphological and functional phenotypic traits, including host genetics (using 354 single nucleotide polymorphisms) and surface-associated microbial communities (using 16S rRNA gene amplicon sequencing) from 160 individuals sampled from eight sites spanning Phyllospora's entire latitudinal distribution (1,300 km). Combined, these factors explained 54% of the overall variation in Phyllospora's associated microbial community structure, much of which was related to the local environment (~32%). We found that putative "core" microbial taxa (i.e., present on all Phyllospora individuals sampled) exhibited slightly higher associations with host traits when compared to "variable" taxa (not present on all individuals). We identified several key genetic loci and phenotypic traits in Phyllospora that were strongly related to multiple microbial amplicon sequence variants, including taxa with known associations to seaweed defence, disease and tissue degradation. This information on how host-associated microbial communities vary with host traits and the environment enhances our current understanding of how "holobionts" (hosts plus their microbiota) are structured. Such understanding can be used to inform management strategies of these important and vulnerable habitats.
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Microbiota , Phaeophyceae , Algas Marinas , Geografía , Microbiota/genética , Phaeophyceae/genética , Fenotipo , ARN Ribosómico 16S/genética , Algas Marinas/genéticaRESUMEN
Preserving biodiversity over time is a pressing challenge for conservation science. A key goal of marine protected areas (MPAs) is to maintain stability in species composition, via reduced turnover, to support ecosystem function. Yet, this stability is rarely measured directly under different levels of protection. Rather, evaluations of MPA efficacy generally consist of static measures of abundance, species richness, and biomass, and rare measures of turnover are limited to short-term studies involving pairwise (beta diversity) comparisons. Zeta diversity is a recently developed metric of turnover that allows for measurement of compositional similarity across multiple assemblages and thus provides more comprehensive estimates of turnover. We evaluated the effectiveness of MPAs at preserving fish zeta diversity across a network of marine reserves over 10 years in Batemans Marine Park, Australia. Snorkel transect surveys were conducted across multiple replicated and spatially interspersed sites to record fish species occurrence through time. Protection provided by MPAs conferred greater stability in fish species turnover. Marine protected areas had significantly shallower decline in zeta diversity compared with partially protected and unprotected areas. The retention of harvested species was four to six times greater in MPAs compared with partially protected and unprotected areas, and the stabilizing effects of protection were observable within 4 years of park implementation. Conversely, partial protection offered little to no improvement in stability, compared with unprotected areas. These findings support the efficacy of MPAs for preserving temporal fish diversity stability. The implementation of MPAs helps stabilize fish diversity and may, therefore, support biodiversity resilience under ongoing environmental change.
Impactos de las Áreas Protegidas Marinas sobre la Estabilidad Temporal de la Diversidad de Especies de Peces Resumen A medida que avanza el tiempo, la conservación de la biodiversidad es un reto apremiante para las ciencias de la conservación. Un objetivo importante de las áreas marinas protegidas (AMP) es mantener la estabilidad de la composición de especies, por medio de rotaciones reducidas, para así ayudar a la función del ecosistema. Sin embargo, esta estabilidad casi no se mide directamente bajo diferentes niveles de protección. En su lugar, las evaluaciones de eficiencia de las AMP generalmente consisten en medidas estáticas de abundancia, riqueza de especies y biomasa, y las pocas medidas de la rotación están limitadas a los estudios a corto plazo que involucran comparaciones por pares (diversidad beta). La diversidad zeta es una medida recientemente desarrollada de la rotación, la cual permite la medición de las similitudes en la composición en múltiples ensamblajes, proporcionando así estimaciones más completas de la rotación. Evaluamos la efectividad que tienen las AMP en la conservación de la diversidad zeta de los peces en una red de reservas marinas durante diez años en el Parque Marino Bateman, Australia. Se realizaron censos en transecto con snorkel en varios sitios replicados e intercalados espacialmente para registrar la presencia de especies de peces a lo largo del tiempo. La protección proporcionada por las AMP otorgó una mayor estabilidad en la rotación de especies de peces. Las áreas marinas protegidas tuvieron una declinación significativamente más baja de la diversidad zeta que las áreas parcialmente protegidas o desprotegidas. La retención de especies pescadas fue 4-6 veces mayor en las AMP que en las áreas desprotegidas o parcialmente protegidas, y los efectos estabilizadores de la protección fueron observables a partir de cuatro años de la implementación del parque. De manera opuesta, la protección parcial ofreció poca o ninguna estabilidad, comparada con las áreas desprotegidas. Estos descubrimientos respaldan la eficiencia que tienen las AMP en la conservación de la estabilidad temporal de la diversidad de especies de peces. La implementación de las AMP ayuda a estabilizar la diversidad de peces y por lo tanto puede fomentar la resiliencia de la biodiversidad frente al cambio ambiental en curso.
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Conservación de los Recursos Naturales , Ecosistema , Animales , Australia , Biodiversidad , PecesRESUMEN
Coastal systems such as estuaries are threatened by multiple anthropogenic stressors worldwide. However, how these stressors and estuarine hydrology shape benthic bacterial communities and their functions remains poorly known. Here, we surveyed sediment bacterial communities in poorly flushed embayments and well flushed channels in Sydney Harbour, Australia, using 16S rRNA gene sequencing. Sediment samples were collected monthly during the Austral summer-autumn 2014 at increasing distance from a large storm drain in each channel and embayment. Bacterial communities differed significantly between sites that varied in proximity to storm drains, with a gradient of change apparent for sites within embayments. We explored this pattern for embayment sites with analysis of RNA-Seq gene expression patterns and found higher expression of multiple genes involved in bacterial stress response far from storm drains, suggesting that bacterial communities close to storm drains may be more tolerant of localised anthropogenic stressors. Several bacterial groups also differed close to and far from storm drains, suggesting their potential utility as bioindicators to monitor contaminants in estuarine sediments. Overall, our study provides useful insights into changes in the composition and functioning of benthic bacterial communities as a result of multiple anthropogenic stressors in differing hydrological conditions.