Characterization and comparison of bacterial communities of an invasive and two native Caribbean seagrass species sheds light on the possible influence of the microbiome on invasive mechanisms

Invasive plants, including marine macrophytes, are one of the most important threats to biodiversity by displacing native species and organisms depending on them. Invasion success is dependent on interactions among living organisms, but their study has been mostly limited to negative interactions while positive interactions are mostly underlooked. Recent studies suggested that microorganisms associated with eukaryotic hosts may play a determinant role in the invasion process. Along with the knowledge of their structure, taxonomic composition, and potential functional profile, understanding how bacterial communities are associated with the invasive species and the threatened natives (species-specific/environmentally shaped/tissue-specific) can give us a holistic insight into the invasion mechanisms. Here, we aimed to compare the bacterial communities associated with leaves and roots of two native Caribbean seagrasses (Halodule wrightii and Thalassia testudinum) with those of the successful invader Halophila stipulacea, in the Caribbean island Curaçao, using 16S rRNA gene amplicon sequencing and functional prediction. Invasive seagrass microbiomes were more diverse and included three times more species-specific core OTUs than the natives. Associated bacterial communities were seagrass-specific, with higher similarities between natives than between invasive and native seagrasses for both communities associated with leaves and roots, despite their strong tissue differentiation. However, with a higher number of OTUs in common, the core community (i.e., OTUs occurring in at least 80% of the samples) of the native H. wrightii was more similar to that of the invader H. stipulacea than T. testudinum, which could reflect more similar essential needs (e.g., nutritional, adaptive, and physiological) between native and invasive, in contrast to the two natives that might share more environment-related OTUs. Relative to native seagrass species, the invasive H. stipulacea was enriched in halotolerant bacterial genera with plant growth-promoting properties (like Halomonas sp. and Lysinibacillus sp.) and other potential beneficial effects for hosts (e.g., heavy metal detoxifiers and quorum sensing inhibitors). Predicted functional profiles also revealed some advantageous traits on the invasive species such as detoxification pathways, protection against pathogens, and stress tolerance. Despite the predictive nature of our findings concerning the functional potential of the bacteria, this investigation provides novel and important insights into native vs. invasive seagrasses microbiome. We demonstrated that the bacterial community associated with the invasive seagrass H. stipulacea is different from native seagrasses, including some potentially beneficial bacteria, suggesting the importance of considering the microbiome dynamics as a possible and important influencing factor in the colonization of non-indigenous species. We suggest further comparison of H. stipulacea microbiome from its native range with that from both the Mediterranean and Caribbean habitats where this species has a contrasting invasion success. Also, our new findings open doors to a more in-depth investigation combining meta-omics with bacterial manipulation experiments in order to confirm any functional advantage in the microbiome of this invasive seagrass.CEECINST/00114/2018info:eu-repo/semantics/publishedVersio

Some don't like it hot: microhabitat-dependent thermal and water stresses in a trailing edge population

The distributional limits of species in response to environmental change are usually studied at large temporal and/or geographical scales. However, organismal scale habitat variation can be overlooked when investigating large-scale averages of key factors such as temperature. We examine how microhabitat thermal conditions relate to physiological limits, which may contribute to recent range shifts in an intertidal alga. We defined the onset and maximum temperatures of the heat-shock response (HSR) for a southern edge population of Fucus vesiculosus, which has subsequently become extinct. The physiological threshold for resilience (assayed using chlorophyll fluorescence) coincided with declining HSR, determined from the temperature-dependent induction of seven heat-shock protein transcripts. In intertidal habitats, temperature affects physiology directly by controlling body temperature and indirectly through evaporative water loss. We investigated the relationship between the thermal environment and in situ molecular HSR at microhabitat scales. Over cm to m scales, four distinct microhabitats were defined in algal patches (canopy surface, patch edge, subcanopy, submerged channels), revealing distinct thermal and water stress environments during low-tide emersion. The in situ HSR agreed with estimated tissue temperatures in all but one microhabitat. Remarkably, in the most thermally extreme microhabitat (canopy surface), the HSR was essentially absent in desiccated tissue, providing a potential escape from the cellular metabolic costs of thermal stress. Meteorological records, microenvironmental thermal profiles and HSR data indicate that the maximum HSR is approached or exceeded in hydrated tissue during daytime low tides for much of the year. Furthermore, present-day summer seawater temperatures are sufficient to induce HSR during high-tide immersion, preventing recovery and resulting in continuous HSR during daytime low-tide cycles over the entire summer. HSR in the field matched microhabitat temperatures more closely than local seawater or atmospheric data, suggesting that the impacts of climatic change are best understood at the microhabitat scale, particularly in intertidal areas.FCT - Portuguese Science Foundation [POCTI/MAR/61105/2004, EXCL/AAG-GLO/0661/2012, SFRH/BPD/63/03/2009, SFRH/BD/74436/2010]info:eu-repo/semantics/publishedVersio

Interactions between seagrasses and seaweeds during surge nitrogen acquisition determine interspecific competition

Seagrasses dominate shallow coastal environments where nitrogen (N) availability in the water column is often sporadic and mainly in the form of pulses. We investigated the N uptake competition between seagrasses and seaweeds through a series of N-15 surge uptake experiments combining single-species and mixed incubations across ammonium concentrations. N surge uptake rates of seagrasses were 2 to 14-fold higher than those of seaweeds in the majority of combinations, showing that seagrasses are generally in a competitive advantage over seaweeds in N-poor environments with N-pulses. No threshold concentration of ammonium was found beyond which seaweeds performed better than seagrasses. Mixed incubations revealed interspecific interactions that affected rates positively and negatively. Uptake rates obtained in single-species incubations, therefore, cannot always be used to predict the outcome of uptake competition. Only two (Zostera marina vs. Ulva rotundata and Zostera marina vs. Codium decorticatum) of the nine combinations tested (Z. marina, Z. noltei and Cymodocea nodosa vs. U. rotundata, C. decorticatum and Dictyota dichotoma) were found to enhance macroalgal uptake. Our results showed that the surge uptake capacity of seagrasses represents an important mechanism in their N acquisition strategy that justifies their dominance in shallow oligotrophic environments.Portuguese Foundation for Science and Technology (FCT) [PTDC/MAR/098069/2008, SFRH/BPD/63703/2009]; FCT - Foundation for Science and Technology [CCMAR/Multi/04326/2013

Response of kelps from different latitudes to consecutive heat shock

Although extensive work has focused on kelp responses to constant temperature, little is known about their response to the consecutive temperature shocks they are often exposed to in the shallow subtidal and intertidal pools. Here we characterized the responses of the two southernmost forest-forming kelp species in the Northeast Atlantic, Laminaria ochroleuca De La Pylaie and Saccorhiza polyschides (Lightf.) Batt. to multiple cycles of thermal stress. Individuals from the upper vertical limit of the geographical distribution edges where the two species co-occur forming forests, France and Portugal, were exposed to 4 consecutive cycles of thermal shock simulating a spring tide. A 24 h cycle consisted of culture at 15 degrees C, plus 1 h heat shock at one of five levels (20, 22.5, 25, 27.5 or 30 degrees C). The maximum quantum yield (Fv/Fm) of chlorophyll fluorescence of photosystem 2 (PS2) was used to detect impaired reaction center function, as a proxy for individual fitness costs, during recovery from heat shock. Both species showed resilience to temperatures from 20 to 25 degrees C. While exposure to 27.5 degrees C caused no inhibition to Fv/Fm of S. polyschides, a threshold was met above this temperature and exposure to 30 degrees C caused the death of all individuals. In contrast, L ochroleuca from France was damaged but able to survive 30 degrees C shocks and individuals from Portugal showed complete resilience to this treatment. In both species, blade elongation decreased with increasing temperature, with necrosis surpassing growth at higher temperatures. Resilience to high temperature exposure may confer an advantage to L ochroleuca to colonize intertidal pools on the Portuguese coast, in agreement with the observation that both species recruit in tide pools but only L ochroleuca reach adulthood. Our results indicate that as summer temperatures increase with climate change, the disappearance of S. polyschides from intertidal pools and a decrease in the density of L ochroleuca can be expected. (C) 2014 Elsevier B.V. All rights reserved.ASSEMBLE (ASSociation of European Marine Biological Laboratories) [227799]; Portuguese Science and Technology Foundation (FCT); FCT [PTDC/AAC-CLI/109108/2008, EXCL/AAG-GLO/0661/2012]info:eu-repo/semantics/publishedVersio

Fast sporophyte replacement after removal suggests banks of latent microscopic stages of Laminaria ochroleuca (Phaeophyceae) in tide pools in northern Portugal. Cahiers de Biologie

Abstract: This study investigated the effects of a physical disturbance consisting of the removal of adult kelps (Laminaria ochroleuca Bachelot de la Pylaie) and their corresponding understorey turf assemblage in tide pools in northern Portugal. Vertical plots of 0.25 m 2 were scraped in April 2007 in independent tide pools and were monitored one (May) and four (August) months after removal. A rapid sporophyte development was observed in the disturbed plots, attaining mean densities of 40 and 82 young sporophytes.m -2 one and four months after disturbance, respectively. Mean blade lengths in August reached 14.97 ± 7.10 cm. The observed recruitment seemed to be the result of a (resumed) development of microscopic forms present on the substrate in a state of suspended growth. These findings suggest the existence of a bank of microscopic forms capable of replacing populations subject to severe physical disturbances, such as dislodgement by winter storms. Whether such a microscopic bank is mainly composed by spores, gametophytes or early sporophyte stages remains unknown. Résumé : Le rapide remplacement de sporophytes après éradicaion suggèrel'existence d'une banque de formes microscopiques chez Laminaria ochroleuca (Phaeophiceae) dans les cuvettes du Nord Portugal. Cette étude analys les effets de la suppression de laminaires adultes (Laminaria ochroleuca Bachelot de la Pylaie) et de leur communauté de macroalgues associée dans des cuvettes du Nord du Portugal sur le développement de nouveaux sporophytes. En avril 2007, la roche a été grattée au sein de deux cadrats verticaux (0,25 m 2 ), chacun dans une cuvette distincte, qui ont été revisités un mois (en mai) et quatre mois après (en août). Un rapide recrutement de sporophytes a été observé dans les parcelles perturbées, avec un recrutement de laminaires atteignant 40 et 82 recrues.m -2 respectivement un et quatre mois après la destruction. La longueur moyenne des lames en août a atteint 14.97 ± 7.10 cm. Le recrutement observé semble résulter d'une reprise du développement de formes microscopiques présentes sur le substrat dans un état de dormance. Ces résultats suggèrent l'existence d'une banque de formes microscopiques capables de remplacer les populations de sporophytes soumises à de graves perturbations physiques, comme l'arrachage des thalles adultes résultant des tempêtes hivernales, bien que la forme exacte de cette banque microscopique reste inconnue

Seaweed reproductive biology: environmental and genetic controls

Knowledge of life cycle progression and reproduction of seaweeds transcends pure academic interest. Successful and sustainable seaweed exploitation and domestication will indeed require excellent control of the factors controlling growth and reproduction. The relative dominance of the ploidy-phases and their respective morphologies, however, display tremendous diversity. Consequently, the ecological and endogenous factors controlling life cycles are likely to be equally varied. A vast number of research papers addressing theoretical, ecological and physiological aspects of reproduction have been published over the years. Here, we review the current knowledge on reproductive strategies, trade-offs of reproductive effort in natural populations, and the environmental and endogenous factors controlling reproduction. Given that the majority of ecophysiological studies predate the "-omics" era, we examine the extent to which this knowledge of reproduction has been, or can be, applied to further our knowledge of life cycle control in seaweeds.European Commission [FA1406]; China Scholarship Council [201504910698]; Ghent University BOF Special Research Fund [01SC2316]; FCT fellowship [SFRH/BPD/107878/2015]info:eu-repo/semantics/publishedVersio

Haploid females in the isomorphic biphasic life-cycle of Gracilaria chilensis excel in survival

Background Conditional differentiation is one of the most fundamental drivers of biodiversity. Competitive entities (usually species) differ in environmental or ecological niche enabling them to co-exist. Conditional differentiation of haploid and diploid generations is considered to be a requirement for the evolutionary stability of isomorphic biphasic life-cycles and the cause for the natural occurrence of both phases at uneven abundances. Theoretically, stage dependent survival rates are the most efficient way to explain conditional differentiation. Results We tested for conditional differentiation in survival rates among life stages (haploid males, haploid females, and diploids) of Gracilaria chilensis, an intertidal red alga occurring along the Chilean shores. Therefore, the fate of individuals was followed periodically for 3 years in five intertidal pools and, for the first time in isomorphic red algae, a composite model of the instantaneous survival rates was applied. The results showed the survival dependency on density (both competition and Allee effects), fertility, age, size, season and location, as well as the differentiation among stages for the survival dependencies of these factors. The young haploid females survived more than the young of the other stages under Allee effects during the environmentally stressful season at the more exposed locations, and under self-thinning during the active growth season. Furthermore, fertile haploid females had a higher survival than fertile haploid males or fertile diploids. Conclusions Here, we show a survival advantage of haploids over diploids. The haploid females probably optimize their resource management targeting structural and physiological adaptations that significantly enhance survival under harsher conditions. In a companion paper we demonstrate a fertility advantage of diploids over haploids. Together, the survival and fertility differentiation support the evolution and prevalence of biphasic life-cycles.info:eu-repo/semantics/publishedVersio

Record of the first Pleonexes species (Crustacea: Amphipoda: Ampithoidae) in Moroccan waters: Pleonexes gammaroides Spence Bate, 1857

The ampithoid amphipod crustacean Pleonexes gammaroides Spence Bate, 1857 is reported from Morocco (northeastern Atlantic Ocean) for the first time, where it is the only representative of the genus Pleonexes Spence Bate, 1857 so far. Specimens were collected from the upper fringe of the infralittoral zone (including low intertidal) of El Jadida coastline associated with the holdfasts of the kelp Saccorhiza polyschides (Lightfoot) Batters (Phaeophyceae), colonising the sublittoral fringe in the southernmost distribution limit (Morocco). This finding updates the known geographical distribution of P. gammaroides in northern Africa and northeastern Atlantic. Some ecological and distributional details of this amphipod species are briefly discussed here.National Centre for Scientific and Technical Research (CNRST), Morocco 5UCD2017, AGA- KHAN Foundation under the project MARAFRICA AGA-KHAN/540316524/2019info:eu-repo/semantics/publishedVersio

Marine forests of the Mediterranean-Atlantic Cystoseira tamariscifolia complex show a southern Iberian genetic hotspot and no reproductive isolation in parapatry

Climate-driven range-shifts create evolutionary opportunities for allopatric divergence and subsequent contact, leading to genetic structuration and hybrid zones. We investigate how these processes influenced the evolution of a complex of three closely related Cystoseira spp., which are a key component of the Mediterranean-Atlantic seaweed forests that are undergoing population declines. The C. tamariscifolia complex, composed of C. tamariscifolia s.s., C. amentacea and C. mediterranea, have indistinct boundaries and natural hybridization is suspected. Our aims are to (1) infer the genetic structure and diversity of these species throughout their distribution ranges using microsatellite markers to identify ancient versus recent geographical populations, contact zones and reproductive barriers, and (2) hindcast past distributions using niche models to investigate the influence of past range shifts on genetic divergence at multiple spatial scales. Results supported a single, morphologically plastic species the genetic structure of which was incongruent with a priori species assignments. The low diversity and low singularity in northern European populations suggest recent colonization after the LGM. The southern Iberian genetic hotspot most likely results from the role of this area as a climatic refugium or a secondary contact zone between differentiated populations or both. We hypothesize that life-history traits (selfing, low dispersal) and prior colonization effects, rather than reproductive barriers, might explain the observed genetic discontinuities.Pew Charitable Trusts (USA); MARINERA, Spain [CTM2008-04183-E/MAR]; FCT (Portugal) [FCT-BIODIVERSA/004/2015, CCMAR/Multi/04326/2013, SFRH/BPD/107878/2015, SFRH/BPD/85040/2012]; FPU fellowship of the Spanish Ministry of Education; European Community ASSEMBLE visiting grant [00399/2012]; University of Cadi

A Meta-Analysis of Seaweed Impacts on Seagrasses: Generalities and Knowledge Gaps

Seagrasses are important habitat-formers and ecosystem engineers that are under threat from bloom-forming seaweeds. These seaweeds have been suggested to outcompete the seagrasses, particularly when facilitated by eutrophication, causing regime shifts where green meadows and clear waters are replaced with unstable sediments, turbid waters, hypoxia, and poor habitat conditions for fishes and invertebrates. Understanding the situations under which seaweeds impact seagrasses on local patch scales can help proactive management and prevent losses at greater scales. Here, we provide a quantitative review of available published manipulative experiments (all conducted at the patch-scale), to test which attributes of seaweeds and seagrasses (e.g., their abundances, sizes, morphology, taxonomy, attachment type, or origin) influence impacts. Weighted and unweighted meta-analyses (Hedges d metric) of 59 experiments showed generally high variability in attribute-impact relationships. Our main significant findings were that (a) abundant seaweeds had stronger negative impacts on seagrasses than sparse seaweeds, (b) unattached and epiphytic seaweeds had stronger impacts than ‘rooted’ seaweeds, and (c) small seagrass species were more susceptible than larger species. Findings (a) and (c) were rather intuitive. It was more surprising that ‘rooted’ seaweeds had comparatively small impacts, particularly given that this category included the infamous invasive Caulerpa species. This result may reflect that seaweed biomass and/or shading and metabolic by-products like anoxia and sulphides could be lower for rooted seaweeds. In conclusion, our results represent simple and robust first-order generalities about seaweed impacts on seagrasses. This review also documented a limited number of primary studies. We therefore identified major knowledge gaps that need to be addressed before general predictive models on seaweed-seagrass interactions can be build, in order to effectively protect seagrass habitats from detrimental competition from seaweeds