Effect of marine heatwaves and warming on kelp microbiota influence trophic interactions.

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.

Is the Intestinal Bacterial Community in the Australian Rabbitfish Siganus fuscescens Influenced by Seaweed Supplementation or Geography?

We recently demonstrated that dietary supplementation with seaweed leads to dramatic improvements in immune responses in S. fuscescens, a candidate species for aquaculture development in Asia. Here, to assess whether the immunostimulatory effect was facilitated by changes to the gut microbiome, we investigated the effects of those same seaweed species and four commercial feed supplements currently used in aquaculture on the bacterial communities in the hindgut of the fish. Since we found no correlations between the relative abundance of any particular taxa and the fish enhanced innate immune responses, we hypothesised that S. fuscescens might have a core microbiome that is robust to dietary manipulation. Two recently published studies describing the bacteria within the hindgut of S. fuscescens provided an opportunity to test this hypothesis and to compare our samples to those from geographically distinct populations. We found that, although hindgut bacterial communities were clearly and significantly distinguishable between studies and populations, a substantial proportion (55 of 174 taxa) were consistently detected across all populations. Our data suggest that the importance of gut microbiota to animal health and the extent to which they can be influenced by dietary manipulations might be species-specific or related to an animals' trophic level.

Host genetics, phenotype and geography structure the microbiome of a foundational seaweed.

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.

Seaweed dietary supplements enhance the innate immune response of the mottled rabbitfish, Siganus fuscescens.

Disease is one of the major bottlenecks for aquaculture development, costing the industry in excess of US $6 billion each year. The increase in pressure to phase out some traditional approaches to disease control (e.g. antibiotics) is pushing farmers to search for alternatives to treat and prevent disease outbreaks, which do not have detrimental consequences (e.g. antibiotic resistance). We tested the effects of eleven seaweed species and four established fish immunostimulants on the innate immune response (cellular and humoral immunity) of the rabbitfish Siganus fuscescens. All supplements including different seaweeds from the three groups (Chlorophyta, Phaeophyta and Rhodophyta) were included in the fish pellet at 3% (by weight) and had variably positive effects across the four innate immune parameters we measured compared to control fish. Diets supplemented with the red seaweed Asparagopsis taxiformis and the brown seaweed Dictyota intermedia led to the largest boosts in humoral and cellular innate immune defences, including particularly significant increases in haemolytic activity. Diets supplemented with Ulva fasciata also led to promising positive effects on the fish innate immune responses. We conclude that dietary seaweed supplements can boost the immune response of S. fuscescens and thus the top three species highlighted in this study should be further investigated for this emerging aquaculture species and other fish species.

Application of omics research in seaweeds with a focus on red seaweeds.

Targeted 'omics' research for seaweeds, utilizing various computational and informatics frameworks, has the potential to rapidly develop our understanding of biological processes at the molecular level and contribute to solutions for the most pressing environmental and social issues of our time. Here, a systematic review into the current status of seaweed omics research was undertaken to evaluate the biological diversity of seaweed species investigated (red, green and brown phyla), the levels to which the work was undertaken (from full genome to transcripts, proteins or metabolites) and the field of research to which it has contributed. We report that from 1994 to 2021 the majority of seaweed omics research has been performed on the red seaweeds (45% of total studies), with more than half of these studies based upon two genera Pyropia and Gracilaria. A smaller number of studies examined brown seaweed (key genera Saccharina and Sargassum) and green seaweed (primarily Ulva). Overall, seaweed omics research is most highly associated with the field of evolution (46% of total studies), followed by the fields of ecology, natural products and their biosynthesis, omics methodology and seaweed-microbe interactions. Synthesis and specific outcomes derived from omics studies in the red seaweeds are provided. Together, these studies have provided a broad-scale interrogation of seaweeds, facilitating our ability to answer fundamental queries and develop applied outcomes. Crucial to the next steps will be establishing analytical tools and databases that can be more broadly utilized by practitioners and researchers across the globe because of their shared interest in the key seaweed genera.

Genomic vulnerability of a dominant seaweed points to future-proofing pathways for Australia's underwater forests.

Globally, critical habitats are in decline, threatening ecological, economic and social values and prompting calls for 'future proofing' efforts that enhance resilience to climate change. Such efforts rely on predicting how neutral and adaptive genomic patterns across a species' distribution will change under future climate scenarios, but data is scant for most species of conservation concern. Here, we use seascape genomics to characterise genetic diversity, structure and gene-environmental associations in a dominant forest-forming seaweed, Phyllospora comosa, along its entire latitudinal (12° latitude), and thermal (~14°C) range. Phyllospora showed high connectivity throughout its central range, with evidence of genetic structure and potential selection associated with sea surface temperatures (SSTs) at its rear and leading edges. Rear and leading-edge populations harboured only half the genetic diversity of central populations. By modelling genetic turnover as a function of SST, we assessed the genomic vulnerability across Phyllospora's distributional range under climate change scenarios. Despite low diversity, range-edge populations were predicted to harbour beneficial adaptations to marginal conditions and overall adaptability of the species may be compromised by their loss. Assisted gene flow from range edge populations may be required to enhance adaptation and increase resilience of central and leading-edge populations under warming oceans. Understanding genomic vulnerability can inform proactive restoration and future-proofing strategies for underwater forests and ensure their persistence in changing oceans.

Kelp forests.

Vergés and Campbell introduce the kelp forest ecosystem.

Genomic, metabolic and phenotypic variability shapes ecological differentiation and intraspecies interactions of Alteromonas macleodii.

Ecological differentiation between strains of bacterial species is shaped by genomic and metabolic variability. However, connecting genotypes to ecological niches remains a major challenge. Here, we linked bacterial geno- and phenotypes by contextualizing pangenomic, exometabolomic and physiological evidence in twelve strains of the marine bacterium Alteromonas macleodii, illuminating adaptive strategies of carbon metabolism, microbial interactions, cellular communication and iron acquisition. In A. macleodii strain MIT1002, secretion of amino acids and the unique capacity for phenol degradation may promote associations with Prochlorococcus cyanobacteria. Strain 83-1 and three novel Pacific isolates, featuring clonal genomes despite originating from distant locations, have profound abilities for algal polysaccharide utilization but without detrimental implications for Ecklonia macroalgae. Degradation of toluene and xylene, mediated via a plasmid syntenic to terrestrial Pseudomonas, was unique to strain EZ55. Benzoate degradation by strain EC673 related to a chromosomal gene cluster shared with the plasmid of A. mediterranea EC615, underlining that mobile genetic elements drive adaptations. Furthermore, we revealed strain-specific production of siderophores and homoserine lactones, with implications for nutrient acquisition and cellular communication. Phenotypic variability corresponded to different competitiveness in co-culture and geographic distribution, indicating linkages between intraspecific diversity, microbial interactions and biogeography. The finding of "ecological microdiversity" helps understanding the widespread occurrence of A. macleodii and contributes to the interpretation of bacterial niche specialization, population ecology and biogeochemical roles.

A horizon scan of priorities for coastal marine microbiome research.

Research into the microbiomes of natural environments is changing the way ecologists and evolutionary biologists view the importance of microorganisms in ecosystem function. This is particularly relevant in ocean environments, where microorganisms constitute the majority of biomass and control most of the major biogeochemical cycles, including those that regulate Earth's climate. Coastal marine environments provide goods and services that are imperative to human survival and well-being (for example, fisheries and water purification), and emerging evidence indicates that these ecosystem services often depend on complex relationships between communities of microorganisms (the 'microbiome') and the environment or their hosts - termed the 'holobiont'. Understanding of coastal ecosystem function must therefore be framed under the holobiont concept, whereby macroorganisms and their associated microbiomes are considered as a synergistic ecological unit. Here, we evaluate the current state of knowledge on coastal marine microbiome research and identify key questions within this growing research area. Although the list of questions is broad and ambitious, progress in the field is increasing exponentially, and the emergence of large, international collaborative networks and well-executed manipulative experiments are rapidly advancing the field of coastal marine microbiome research.

Measuring continuous compositional change using decline and decay in zeta diversity.

Incidence, or compositional, matrices are generated for a broad range of research applications in biology. Zeta diversity provides a common currency and conceptual framework that links incidence-based metrics with multiple patterns of interest in biology, ecology, and biodiversity science. It quantifies the variation in species (or OTU) composition of multiple assemblages (or cases) in space or time, to capture the contribution of the full suite of narrow, intermediate, and wide-ranging species to biotic heterogeneity. Here we provide a conceptual framework for the application and interpretation of patterns of continuous change in compositional diversity using zeta diversity. This includes consideration of the survey design context, and the multiple ways in which zeta diversity decline and decay can be used to examine and test turnover in the identity of elements across space and time. We introduce the zeta ratio-based retention rate curve to quantify rates of compositional change. We illustrate these applications using 11 empirical data sets from a broad range of taxa, scales, and levels of biological organization-from DNA molecules and microbes to communities and interaction networks-including one of the original data sets used to express compositional change and distance decay in ecology. We show (1) how different sample selection schemes used during the calculation of compositional change are appropriate for different data types and questions, (2) how higher orders of zeta may in some cases better detect shifts and transitions, and (3) the relative roles of rare vs. common species in driving patterns of compositional change. By exploring the application of zeta diversity decline and decay, including the retention rate, across this broad range of contexts, we demonstrate its application for understanding continuous turnover in biological systems.

Future climate change is predicted to affect the microbiome and condition of habitat-forming kelp.

Climate change is driving global declines of marine habitat-forming species through physiological effects and through changes to ecological interactions, with projected trajectories for ocean warming and acidification likely to exacerbate such impacts in coming decades. Interactions between habitat-formers and their microbiomes are fundamental for host functioning and resilience, but how such relationships will change in future conditions is largely unknown. We investigated independent and interactive effects of warming and acidification on a large brown seaweed, the kelp Ecklonia radiata, and its associated microbiome in experimental mesocosms. Microbial communities were affected by warming and, during the first week, by acidification. During the second week, kelp developed disease-like symptoms previously observed in the field. The tissue of some kelp blistered, bleached and eventually degraded, particularly under the acidification treatments, affecting photosynthetic efficiency. Microbial communities differed between blistered and healthy kelp for all treatments, except for those under future conditions of warming and acidification, which after two weeks resembled assemblages associated with healthy hosts. This indicates that changes in the microbiome were not easily predictable as the severity of future climate scenarios increased. Future ocean conditions can change kelp microbiomes and may lead to host disease, with potentially cascading impacts on associated ecosystems.

Interactions within the microbiome alter microbial interactions with host chemical defences and affect disease in a marine holobiont.

Our understanding of diseases has been transformed by the realisation that people are holobionts, comprised of a host and its associated microbiome(s). Disease can also have devastating effects on populations of marine organisms, including dominant habitat formers such as seaweed holobionts. However, we know very little about how interactions between microorganisms within microbiomes - of humans or marine organisms - affect host health and there is no underpinning theoretical framework for exploring this. We applied ecological models of succession to bacterial communities to understand how interactions within a seaweed microbiome affect the host. We observed succession of surface microbiomes on the red seaweed Delisea pulchra in situ, following a disturbance, with communities 'recovering' to resemble undisturbed states after only 12 days. Further, if this recovery was perturbed, a bleaching disease previously described for this seaweed developed. Early successional strains of bacteria protected the host from colonisation by a pathogenic, later successional strain. Host chemical defences also prevented disease, such that within-microbiome interactions were most important when the host's chemical defences were inhibited. This is the first experimental evidence that interactions within microbiomes have important implications for host health and disease in a dominant marine habitat-forming organism.

Long-term empirical evidence of ocean warming leading to tropicalization of fish communities, increased herbivory, and loss of kelp.

Some of the most profound effects of climate change on ecological communities are due to alterations in species interactions rather than direct physiological effects of changing environmental conditions. Empirical evidence of historical changes in species interactions within climate-impacted communities is, however, rare and difficult to obtain. Here, we demonstrate the recent disappearance of key habitat-forming kelp forests from a warming tropical-temperate transition zone in eastern Australia. Using a 10-y video dataset encompassing a 0.6 °C warming period, we show how herbivory increased as kelp gradually declined and then disappeared. Concurrently, fish communities from sites where kelp was originally abundant but subsequently disappeared became increasingly dominated by tropical herbivores. Feeding assays identified two key tropical/subtropical herbivores that consumed transplanted kelp within hours at these sites. There was also a distinct increase in the abundance of fishes that consume epilithic algae, and much higher bite rates by this group at sites without kelp, suggesting a key role for these fishes in maintaining reefs in kelp-free states by removing kelp recruits. Changes in kelp abundance showed no direct relationship to seawater temperatures over the decade and were also unrelated to other measured abiotic factors (nutrients and storms). Our results show that warming-mediated increases in fish herbivory pose a significant threat to kelp-dominated ecosystems in Australia and, potentially, globally.

Central and rear-edge populations can be equally vulnerable to warming.

Rear (warm) edge populations are often considered more susceptible to warming than central (cool) populations because of the warmer ambient temperatures they experience, but this overlooks the potential for local variation in thermal tolerances. Here we provide conceptual models illustrating how sensitivity to warming is affected throughout a species' geographical range for locally adapted and non-adapted populations. We test these models for a range-contracting seaweed using observations from a marine heatwave and a 12-month experiment, translocating seaweeds among central, present and historic range edge locations. Growth, reproductive development and survivorship display different temperature thresholds among central and rear-edge populations, but share a 2.5 °C anomaly threshold. Range contraction, therefore, reflects variation in local anomalies rather than differences in absolute temperatures. This demonstrates that warming sensitivity can be similar throughout a species geographical range and highlights the importance of incorporating local adaptation and acclimatization into climate change vulnerability assessments.

Continental-scale variation in seaweed host-associated bacterial communities is a function of host condition, not geography.

Interactions between hosts and associated microbial communities can fundamentally shape the development and ecology of 'holobionts', from humans to marine habitat-forming organisms such as seaweeds. In marine systems, planktonic microbial community structure is mainly driven by geography and related environmental factors, but the large-scale drivers of host-associated microbial communities are largely unknown. Using 16S-rRNA gene sequencing, we characterized 260 seaweed-associated bacterial and archaeal communities on the kelp Ecklonia radiata from three biogeographical provinces spanning 10° of latitude and 35° of longitude across the Australian continent. These phylogenetically and taxonomically diverse communities were more strongly and consistently associated with host condition than geographical location or environmental variables, and a 'core' microbial community characteristic of healthy kelps appears to be lost when hosts become stressed. Microbial communities on stressed individuals were more similar to each other among locations than those on healthy hosts. In contrast to biogeographical patterns of planktonic marine microbial communities, host traits emerge as critical determinants of associated microbial community structure of these holobionts, even at a continental scale.

Spatial variability of microbial assemblages associated with a dominant habitat-forming seaweed.

Macroalgal surfaces support abundant and diverse microorganisms within biofilms, which are often involved in fundamental functions relating to the health and defense of their seaweed hosts, including algal development, facilitation of spore release, and chemical antifouling. Given these intimate and important interactions, environmental changes have the potential to negatively impact macroalgae by disrupting seaweed-microbe interactions. We used the disappearance of the dominant canopy-forming fucoid Phyllospora comosa from the metropolitan coast of Sydney, NSW, Australia as a model system to study these interactions. We transplanted Phyllospora individuals from nearby, extant populations back onto reefs in Sydney to test whether bacterial assemblages associated with seaweed surfaces would be influenced by (i) the host itself, independently of where it occurs, (ii) the type of habitat where the host occurs, or (iii) site-specific differences. Analyses of bacterial DNA fingerprints (terminal fragment length polymorphisms) indicated that assemblages of bacteria on Phyllospora were not habitat-specific. Rather, they were primarily influenced by local, site-specific conditions with some evidence for host-specificity in some cases. This could suggest a lottery model of host-surface colonization, by which hosts are colonized by 'suitable' bacteria available in the local species pool, resulting in high variability in assemblage structure across sites, but where some species in the community are specific to the host and possibly influenced by differences in host traits.

The tropicalization of temperate marine ecosystems: climate-mediated changes in herbivory and community phase shifts.

Climate-driven changes in biotic interactions can profoundly alter ecological communities, particularly when they impact foundation species. In marine systems, changes in herbivory and the consequent loss of dominant habitat forming species can result in dramatic community phase shifts, such as from coral to macroalgal dominance when tropical fish herbivory decreases, and from algal forests to 'barrens' when temperate urchin grazing increases. Here, we propose a novel phase-shift away from macroalgal dominance caused by tropical herbivores extending their range into temperate regions. We argue that this phase shift is facilitated by poleward-flowing boundary currents that are creating ocean warming hotspots around the globe, enabling the range expansion of tropical species and increasing their grazing rates in temperate areas. Overgrazing of temperate macroalgae by tropical herbivorous fishes has already occurred in Japan and the Mediterranean. Emerging evidence suggests similar phenomena are occurring in other temperate regions, with increasing occurrence of tropical fishes on temperate reefs.

Demographic consequences of disease in a habitat-forming seaweed and impacts on interactions between natural enemies.

Diseases affecting natural ecosystems are increasing in frequency and severity, but unless obviously catastrophic, the consequences of disease outbreaks are often overlooked, relative to other ecological processes (e.g., predation, competition). Disease can have profound effects on individuals and can also strongly influence interactions between infected hosts and their natural enemies. We investigated whether a novel bleaching disease affected the survival or performance of a habitat-forming red seaweed, Delisea pulchra. In addition, we investigated bidirectional, multipartite interactions between this seaweed host, its pathogens, and consumers. Although we found no negative impacts of disease on survival of D. pulchra, bleaching had substantial, negative consequences for affected individuals, including a dramatic drop in fecundity and a significant decrease in size. In the first direct demonstration of bacterial disease-mediated herbivory of seaweeds, herbivores generally preferred to consume bleached tissue in feeding trials, and we also found higher densities of herbivores on bleached than co-occurring, healthy algae at sites where herbivores were abundant. In a conceptually reciprocal test of the effects of herbivores on infection, we showed that simulated herbivory increased susceptibility to bleaching when algae were also exposed to cultures of a bacterial pathogen. Given the high proportions of D. pulchra affected by bleaching during peak periods, the impacts of this disease are likely to have important implications at the population level. This work highlights complex interactions between habitat-forming organisms and their natural enemies and further emphasizes the need to consider disease in ecological research.

Towards restoration of missing underwater forests.

Degradation of natural habitats due to urbanization is a major cause of biodiversity loss. Anthropogenic impacts can drive phase shifts from productive, complex ecosystems to less desirable, less diverse systems that provide fewer services. Macroalgae are the dominant habitat-forming organisms on temperate coastlines, providing habitat and food to entire communities. In recent decades, there has been a decline in macroalgal cover along some urbanised shorelines, leading to a shift from diverse algal forests to more simple turf algae or barren habitats. Phyllospora comosa, a major habitat forming macroalga in south-eastern Australia, has disappeared from the urban shores of Sydney. Its disappearance is coincident with heavy sewage outfall discharges along the metropolitan coast during 1970s and 1980s. Despite significant improvements in water-quality since that time, Phyllospora has not re-established. We experimentally transplanted adult Phyllospora into two rocky reefs in the Sydney metropolitan region to examine the model that Sydney is now suitable for the survival and recruitment of Phyllospora and thus assess the possibility of restoring Phyllospora back onto reefs where it was once abundant. Survival of transplanted individuals was high overall, but also spatially variable: at one site most individuals were grazed, while at the other site survival was similar to undisturbed algae and procedural controls. Transplanted algae reproduced and recruitment rates were higher than in natural populations at one experimental site, with high survival of new recruits after almost 18 months. Low supply and settlement success of propagules in the absence of adults and herbivory (in some places) emerge as three potential processes that may have been preventing natural re-establishment of this alga. Understanding of the processes and interactions that shape this system are necessary to provide ecologically sensible goals and the information needed to successfully restore these underwater forests.

Global patterns in the impact of marine herbivores on benthic primary producers.

Despite the importance of consumers in structuring communities, and the widespread assumption that consumption is strongest at low latitudes, empirical tests for global scale patterns in the magnitude of consumer impacts are limited. In marine systems, the long tradition of experimentally excluding herbivores in their natural environments allows consumer impacts to be quantified on global scales using consistent methodology. We present a quantitative synthesis of 613 marine herbivore exclusion experiments to test the influence of consumer traits, producer traits and the environment on the strength of herbivore impacts on benthic producers. Across the globe, marine herbivores profoundly reduced producer abundance (by 68% on average), with strongest effects in rocky intertidal habitats and the weakest effects on habitats dominated by vascular plants. Unexpectedly, we found little or no influence of latitude or mean annual water temperature. Instead, herbivore impacts differed most consistently among producer taxonomic and morphological groups. Our results show that grazing impacts on plant abundance are better predicted by producer traits than by large-scale variation in habitat or mean temperature, and that there is a previously unrecognised degree of phylogenetic conservatism in producer susceptibility to consumption.