High-temperature stress induces bacteria-specific adverse and reversible effects on Ulva (Chlorophyta) growth and its chemosphere in a reductionist model system
Imen Hmani,
Fatemeh Ghaderiardakani,
Leila Ktari
et al.
Abstract:Axenic cultures of the green seaweed Ulva mutabilis were inoculated with bacteria providing essential algal growth and morphogenesis-promoting factors (AGMPFs) and were exposed to temperature shifts from 18 °C to 30 °C. The temperature-dependent effect of bacteria on longitudinal algal growth and the molecular composition of the chemosphere in the algal culture medium was explored. The reductionist tripartite model system of U. mutabilis, Roseovarius sp. MS2, and Maribacter sp. MS6 was applied as a reference a… Show more
“…Microbiome analysis was accompanied by functional examinations to investigate growth and morphogenesis-promoting traits within the microbiome (Hmani et al 2023). For this, bacteria were isolated from the surface of the algal samples using sterile swabs.…”
Section: Identification Of Bacteria That Release Essential Agmpfs Usi...mentioning
confidence: 99%
“…However, these functions may be broadly distributed across various taxonomic groups (Burke et al 2011). In addition, functional characteristics within the same microbiome can also change in a changing environment (Hmani et al 2023). By employing mass spectrometry profiling and imaging techniques, specific metabolic markers have been introduced to visualize the distribution of bacteria (the producers of metabolic markers) on the surface of Ulva spp.…”
Macroalgae are found in a variety of marine vegetation ecosystems around the world, contributing significantly to global net primary production. In particular, the sea lettuce species, i.e., members of the genusUlva(Chlorophyta), are located in many ecological niches and are characterized by excellent adaptability to environmental changes but depend on essential associated bacteria, which release algal growth and morphogenesis-promoting-factors (AGMPFs). Our work investigated the hypothesis that bacteria need to be stress-adapted to provide sufficient amounts of AGMPFs for the growth and morphogenesis ofUlvathroughout its life cycle, even under severe environmental conditions.Our study thus aimed to understand which bacteria contribute to overcoming a variety of stressors in polar regions. Green macroalgae were collected from Potter Cove, King George Island (Isla 25 de Mayo), Antarctica, to study the associated microbiome and, subsequently, to identify AGMPFs releasing bacteria. Therefore, microbiome analysis was combined with morphogenetic bioassays and chemical analysis, identifying bacteria essential for algal growth under Antarctic conditions. Hereby, axenic cultures of a MediterraneanUlva compressa(cultivarUlva mutabilis), previously developed as a model system for bacteria-induced algal growth and morphogenesis, were inoculated with freshly isolated and cultivable Antarctic bacteria to determine their morphogenetic activity.The exploratory microbiome investigation identified numerous cold-adapted AGMPF-producing bacteria. Unlike the reference bacterial strains isolated from the Mediterranean Sea, the cold-adapted isolatesMaribactersp. BPC-D8 andSulfitobactersp. BPC-C4, released sufficient amounts of AGMPFs, such as thallusin, necessary for algal morphogenesis even at 2°C. Our results illustrate the role of chemical mediators provided by bacteria in cross-kingdom interactions under cold conditions within aquatic systems. The newly isolated bacteria will enable further functional studies to understand the resilience of the holobiontUlvaand might applied in algal aquaculture even under adverse conditions. The study highlights the importance of ecophysiological assays in microbiome analysis.
“…Microbiome analysis was accompanied by functional examinations to investigate growth and morphogenesis-promoting traits within the microbiome (Hmani et al 2023). For this, bacteria were isolated from the surface of the algal samples using sterile swabs.…”
Section: Identification Of Bacteria That Release Essential Agmpfs Usi...mentioning
confidence: 99%
“…However, these functions may be broadly distributed across various taxonomic groups (Burke et al 2011). In addition, functional characteristics within the same microbiome can also change in a changing environment (Hmani et al 2023). By employing mass spectrometry profiling and imaging techniques, specific metabolic markers have been introduced to visualize the distribution of bacteria (the producers of metabolic markers) on the surface of Ulva spp.…”
Macroalgae are found in a variety of marine vegetation ecosystems around the world, contributing significantly to global net primary production. In particular, the sea lettuce species, i.e., members of the genusUlva(Chlorophyta), are located in many ecological niches and are characterized by excellent adaptability to environmental changes but depend on essential associated bacteria, which release algal growth and morphogenesis-promoting-factors (AGMPFs). Our work investigated the hypothesis that bacteria need to be stress-adapted to provide sufficient amounts of AGMPFs for the growth and morphogenesis ofUlvathroughout its life cycle, even under severe environmental conditions.Our study thus aimed to understand which bacteria contribute to overcoming a variety of stressors in polar regions. Green macroalgae were collected from Potter Cove, King George Island (Isla 25 de Mayo), Antarctica, to study the associated microbiome and, subsequently, to identify AGMPFs releasing bacteria. Therefore, microbiome analysis was combined with morphogenetic bioassays and chemical analysis, identifying bacteria essential for algal growth under Antarctic conditions. Hereby, axenic cultures of a MediterraneanUlva compressa(cultivarUlva mutabilis), previously developed as a model system for bacteria-induced algal growth and morphogenesis, were inoculated with freshly isolated and cultivable Antarctic bacteria to determine their morphogenetic activity.The exploratory microbiome investigation identified numerous cold-adapted AGMPF-producing bacteria. Unlike the reference bacterial strains isolated from the Mediterranean Sea, the cold-adapted isolatesMaribactersp. BPC-D8 andSulfitobactersp. BPC-C4, released sufficient amounts of AGMPFs, such as thallusin, necessary for algal morphogenesis even at 2°C. Our results illustrate the role of chemical mediators provided by bacteria in cross-kingdom interactions under cold conditions within aquatic systems. The newly isolated bacteria will enable further functional studies to understand the resilience of the holobiontUlvaand might applied in algal aquaculture even under adverse conditions. The study highlights the importance of ecophysiological assays in microbiome analysis.
“…Microorganisms able to flourish in association with macroalgae living in such distinctive and challenging ecological niches are expected to possess unique adaptive mechanisms and diversity. Recently, studies using Chlorophyta Ulva species have shown that the macroalgae‐associated bacterial community, including Actinomycetota, can have beneficial and adverse effects on host growth and development depending on environmental stress conditions (Ghaderiardakani et al, 2017; Hmani et al, 2023). In the single study harnessing exclusively the diversity and bioactive potential of the Actinomycetota culturable community associated with kelp from the northern Portuguese shore, a rich reservoir of taxonomically diverse strains producing antimicrobial and anticancer metabolites was uncovered (Girão et al, 2019).…”
Actinomycetota, associated with macroalgae, remains one of the least explored marine niches. The secondary metabolism of Actinomycetota, the primary microbial source of compounds relevant to biotechnology, continues to drive research into the distribution, dynamics, and metabolome of these microorganisms. In this study, we employed a combination of traditional cultivation and metagenomic analysis to investigate the diversity of Actinomycetota in two native macroalgae species from the Portuguese coast. We obtained and taxonomically identified a collection of 380 strains, which were distributed across 12 orders, 15 families, and 25 genera affiliated with the Actinomycetia class, with Streptomyces making up approximately 60% of the composition. Metagenomic results revealed the presence of Actinomycetota in both Chondrus crispus and Codium tomentosum datasets, with relative abundances of 11% and 2%, respectively. This approach identified 12 orders, 16 families, and 17 genera affiliated with Actinomycetota, with minimal overlap with the cultivation results. Acidimicrobiales emerged as the dominant actinobacterial order in both macroalgae, although no strain affiliated with this taxonomic group was successfully isolated. Our findings suggest that macroalgae represent a hotspot for Actinomycetota. The synergistic use of both culture‐dependent and independent approaches proved beneficial, enabling the identification and recovery of not only abundant but also rare taxonomic members.
Raman spectroscopy was used to study the complex interactions and morphogenesis of the green seaweed Ulva (Chlorophyta) and its associated bacteria under controlled conditions in a reductionist model system. Integrating multiple imaging techniques contributes to a more comprehensive understanding of these biological processes. Therefore, Raman spectroscopy was introduced as a non‐invasive, label‐free tool for examining chemical information of the tripartite community Ulva mutabilis‐Roseovarius sp.‐Maribacter sp. The study explored cell differentiation, cell wall protrusion, and bacterial‐macroalgae interactions of intact algal thalli. Using Raman spectroscopy, the analysis of the CHx‐stretching wavenumber region distinguished spatial regions in Ulva germination and cellular malformations under axenic conditions and upon inoculation with a specific bacterium in bipartite communities. The spectral information was used to guide in‐depth analyses within the fingerprint region and to identify substance classes such as proteins, lipids, and polysaccharides, including evidence for ulvan found in cell wall protrusions.
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