Microorganisms

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13 pages, 1028 KiB

Open AccessArticle

The Prokaryotic Microbiome of Acropora digitifera is Stable under Short-Term Artificial Light Pollution

by Jake Ivan P. Baquiran, Michael Angelou L. Nada, Celine Luisa D. Campos, Sherry Lyn G. Sayco, Patrick C. Cabaitan, Yaeli Rosenberg, Inbal Ayalon, Oren Levy and Cecilia Conaco

Microorganisms 2020, 8(10), 1566; https://doi.org/10.3390/microorganisms8101566 - 12 Oct 2020

Cited by 6 | Viewed by 4009

Abstract

Corals harbor a great diversity of symbiotic microorganisms that play pivotal roles in host nutrition, reproduction, and development. Changes in the ocean environment, such as increasing exposure to artificial light at night (ALAN), may alter these relationships and result in a decline in [...] Read more.

Corals harbor a great diversity of symbiotic microorganisms that play pivotal roles in host nutrition, reproduction, and development. Changes in the ocean environment, such as increasing exposure to artificial light at night (ALAN), may alter these relationships and result in a decline in coral health. In this study, we examined the microbiome associated with gravid specimens of the reef-building coral Acropora digitifera. We also assessed the temporal effects of ALAN on the coral-associated microbial community using high-throughput sequencing of the 16S rRNA gene V4 hypervariable region. The A. digitifera microbial community was dominated by phyla Proteobacteria, Firmicutes, and Bacteroidetes. Exposure to ALAN had no large-scale effect on the coral microbiome, although taxa affiliated with Rhodobacteraceae, Caulobacteraceae, Burkholderiaceae, Lachnospiraceae, and Ruminococcaceae were significantly enriched in corals subjected to ALAN. We further noted an increase in the relative abundance of the family Endozoicomonadaceae (Endozoicomonas) as the spawning period approached, regardless of light treatment. These findings highlight the stability of the A. digitifera microbial community under short-term artificial light pollution and provide initial insights into the response of the collective holobiont to ALAN. Full article

(This article belongs to the Special Issue The Human Epoch: Cnidarians Holobiont Responses from Physiology to Epigenetic)

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17 pages, 1538 KiB

Open AccessArticle

Homogenization of Endosymbiont Communities Hosted by Equatorial Corals during the 2016 Mass Bleaching Event

by Sudhanshi S. Jain, Lutfi Afiq-Rosli, Bar Feldman, Oren Levy, Jun Wei Phua, Benjamin J. Wainwright and Danwei Huang

Microorganisms 2020, 8(9), 1370; https://doi.org/10.3390/microorganisms8091370 - 07 Sep 2020

Cited by 8 | Viewed by 3432

Abstract

Thermal stress drives the bleaching of reef corals, during which the endosymbiotic relationship between Symbiodiniaceae microalgae and the host breaks down. The endosymbiont communities are known to shift in response to environmental disturbances, but how they respond within and between colonies during and [...] Read more.

Thermal stress drives the bleaching of reef corals, during which the endosymbiotic relationship between Symbiodiniaceae microalgae and the host breaks down. The endosymbiont communities are known to shift in response to environmental disturbances, but how they respond within and between colonies during and following bleaching events remains unclear. In 2016, a major global-scale bleaching event hit countless tropical reefs. Here, we investigate the relative abundances of Cladocopium LaJeunesse & H.J.Jeong, 2018 and Durusdinium LaJeunesse, 2018 within and among Pachyseris speciosa colonies in equatorial Singapore that are known to host both these Symbiodiniaceae clades. Bleached and unbleached tissues from bleaching colonies, as well as healthy colonies, during and following the bleaching event were sampled and analyzed for comparison. The nuclear ribosomal internal transcribed spacer (ITS) regions were separately amplified and quantified using a SYBR Green-based quantitative polymerase chain reaction (qPCR) method and Illumina high-throughput sequencing. We found Cladocopium to be highly abundant relative to Durusdinium. The relative abundance of Durusdinium, known to be thermally tolerant, was highest in post-bleaching healthy colonies, while bleached and unbleached tissues from bleaching colonies as well as tissue from healthy colonies during the event had depressed proportions of Durusdinium. Given the importance of Durusdinium for thermal tolerance and stress response, it is surprising that bleached tissue showed limited change over healthy tissue during the bleaching event. Moreover, colonies were invariably dominated by Cladocopium during bleaching, but a minority of colonies were Durusdinium-dominant during non-bleaching times. The detailed characterization of Symbiodiniaceae in specific colonies during stress and recovery will provide insights into this crucial symbiosis, with implications for their responses during major bleaching events. Full article

(This article belongs to the Special Issue The Human Epoch: Cnidarians Holobiont Responses from Physiology to Epigenetic)

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17 pages, 2844 KiB

Open AccessArticle

Gene Expression and Photophysiological Changes in Pocillopora acuta Coral Holobiont Following Heat Stress and Recovery

by Rosa Celia Poquita-Du, Yi Le Goh, Danwei Huang, Loke Ming Chou and Peter A. Todd

Microorganisms 2020, 8(8), 1227; https://doi.org/10.3390/microorganisms8081227 - 12 Aug 2020

Cited by 13 | Viewed by 3977

Abstract

The ability of corals to withstand changes in their surroundings is a critical survival mechanism for coping with environmental stress. While many studies have examined responses of the coral holobiont to stressful conditions, its capacity to reverse responses and recover when the stressor [...] Read more.

The ability of corals to withstand changes in their surroundings is a critical survival mechanism for coping with environmental stress. While many studies have examined responses of the coral holobiont to stressful conditions, its capacity to reverse responses and recover when the stressor is removed is not well-understood. In this study, we investigated among-colony responses of Pocillopora acuta from two sites with differing distance to the mainland (Kusu (closer to the mainland) and Raffles Lighthouse (further from the mainland)) to heat stress through differential expression analysis of target genes and quantification of photophysiological metrics. We then examined how these attributes were regulated after the stressor was removed to assess the recovery potential of P. acuta. The fragments that were subjected to heat stress (2 °C above ambient levels) generally exhibited significant reduction in their endosymbiont densities, but the extent of recovery following stress removal varied depending on natal site and colony. There were minimal changes in chl a concentration and maximum quantum yield (Fv/Fm, the proportion of variable fluorescence (Fv) to maximum fluorescence (Fm)) in heat-stressed corals, suggesting that the algal endosymbionts’ Photosystem II was not severely compromised. Significant changes in gene expression levels of selected genes of interest (GOI) were observed following heat exposure and stress removal among sites and colonies, including Actin, calcium/calmodulin-dependent protein kinase type IV (Camk4), kinesin-like protein (KIF9), and small heat shock protein 16.1 (Hsp16.1). The most responsive GOIs were Actin, a major component of the cytoskeleton, and the adaptive immune-related Camk4 which both showed significant reduction following heat exposure and subsequent upregulation during the recovery phase. Our findings clearly demonstrate specific responses of P. acuta in both photophysiological attributes and gene expression levels, suggesting differential capacity of P. acuta corals to tolerate heat stress depending on the colony, so that certain colonies may be more resilient than others. Full article

(This article belongs to the Special Issue The Human Epoch: Cnidarians Holobiont Responses from Physiology to Epigenetic)

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26 pages, 3211 KiB

Open AccessArticle

Organic Carbon and Nitrogen Isoscapes of Reef Corals and Algal Symbionts: Relative Influences of Environmental Gradients and Heterotrophy

by Takanori Fujii, Yasuaki Tanaka, Koh Maki, Nobue Saotome, Naoko Morimoto, Atsushi Watanabe and Toshihiro Miyajima

Microorganisms 2020, 8(8), 1221; https://doi.org/10.3390/microorganisms8081221 - 11 Aug 2020

Cited by 14 | Viewed by 3242

Abstract

The elemental (C/N) and stable isotopic (δ¹³C, δ¹⁵N) compositions and compound-specific δ¹⁵N values of amino acids (δ¹⁵N_AA) were evaluated for coral holobionts as diagnostic tools to detect spatiotemporal environmental heterogeneity and its effects [...] Read more.

The elemental (C/N) and stable isotopic (δ¹³C, δ¹⁵N) compositions and compound-specific δ¹⁵N values of amino acids (δ¹⁵N_AA) were evaluated for coral holobionts as diagnostic tools to detect spatiotemporal environmental heterogeneity and its effects on coral health. Hermatypic coral samples of eight species were collected at 12 reef sites with differing levels of pollution stress. The C/N ratios, δ¹³C values, and δ¹⁵N values of coral tissues and endosymbiotic algae were determined for 193 coral holobionts, and the amino acid composition and δ¹⁵N_AA values of selected samples were analyzed. δ¹⁵N values were influenced most by pollution stress, while C/N ratios and δ¹³C values depended most strongly on species. The results imply that δ¹³C and δ¹⁵N values are useful indicators for distinguishing the ecological niches of sympatric coral species based on microhabitat preference and resource selectivity. Using δ¹⁵N_AA values, the trophic level (TL) of the examined coral samples was estimated to be 0.71 to 1.53, i.e., purely autotrophic to partially heterotrophic. Significant portions of the variation in bulk δ¹⁵N and δ¹³C values could be explained by the influence of heterotrophy. The TL of symbionts covaried with that of their hosts, implying that amino acids acquired through host heterotrophy are translocated to symbionts. Dependence on heterotrophy was stronger at polluted sites, indicating that the ecological role of corals changes in response to eutrophication. Full article

(This article belongs to the Special Issue The Human Epoch: Cnidarians Holobiont Responses from Physiology to Epigenetic)

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21 pages, 2535 KiB

Open AccessArticle

Proteomic Signatures of Corals from Thermodynamic Reefs

by Anderson B. Mayfield

Microorganisms 2020, 8(8), 1171; https://doi.org/10.3390/microorganisms8081171 - 01 Aug 2020

Cited by 5 | Viewed by 2839

Abstract

Unlike most parts of the world, coral reefs of Taiwan’s deep south have generally been spared from climate change-induced degradation. This has been linked to the oceanographically unique nature of Nanwan Bay, where intense upwelling occurs. Specifically, large-amplitude internal waves cause shifts in [...] Read more.

Unlike most parts of the world, coral reefs of Taiwan’s deep south have generally been spared from climate change-induced degradation. This has been linked to the oceanographically unique nature of Nanwan Bay, where intense upwelling occurs. Specifically, large-amplitude internal waves cause shifts in temperature of 6–9 °C over the course of several hours, and the resident corals not only thrive under such conditions, but they have also been shown to withstand multi-month laboratory incubations at experimentally elevated temperatures. To gain insight into the sub-cellular basis of acclimation to upwelling, proteins isolated from reef corals (Seriatopora hystrix) featured in laboratory-based reciprocal transplant studies in which corals from upwelling and non-upwelling control reefs (<20 km away) were exposed to stable or variable temperature regimes were analyzed via label-based proteomics (iTRAQ). Corals exposed to their “native” temperature conditions for seven days (1) demonstrated highest growth rates and (2) were most distinct from one another with respect to their protein signatures. The latter observation was driven by the fact that two Symbiodiniaceae lipid trafficking proteins, sec1a and sec34, were marginally up-regulated in corals exposed to their native temperature conditions. Alongside the marked degree of proteomic “site fidelity” documented, this dataset sheds light on the molecular mechanisms underlying acclimatization to thermodynamically extreme conditions in situ. Full article

(This article belongs to the Special Issue The Human Epoch: Cnidarians Holobiont Responses from Physiology to Epigenetic)

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11 pages, 1693 KiB

Open AccessArticle

Seasonal Variations in the Culturable Mycobiome of Acropora loripes along a Depth Gradient

by Nofar Lifshitz, Lena Hazanov, Maoz Fine and Oded Yarden

Microorganisms 2020, 8(8), 1139; https://doi.org/10.3390/microorganisms8081139 - 28 Jul 2020

Cited by 4 | Viewed by 2458

Abstract

Coral associated fungi are widespread, highly diverse and are part and parcel of the coral holobiont. To study how environmental conditions prevailing near the coral-host may affect fungal diversity, the culturable (isolated on potato dextrose agar) mycobiome associated with Acropora loripes colonies was [...] Read more.

Coral associated fungi are widespread, highly diverse and are part and parcel of the coral holobiont. To study how environmental conditions prevailing near the coral-host may affect fungal diversity, the culturable (isolated on potato dextrose agar) mycobiome associated with Acropora loripes colonies was seasonally sampled along a depth gradient in the Gulf of Aqaba. Fragments were sampled from both apparently healthy coral colonies as well as those exhibiting observable lesions. Based on phylogenetic analysis of 197 fungal sequences, Ascomycota were the most prevalent (91.9%). The abundance of fungi increased with increasing water depth, where corals sampled at 25 m yielded up to 70% more fungal colony forming units (CFUs) than those isolated at 6 m. Fungal diversity at 25 m was also markedly higher, with over 2-fold more fungal families represented. Diversity was also higher in lesioned coral samples, when compared to apparently healthy colonies. In winter, concurrent with water column mixing and increased levels of available nutrients, at the shallow depths, Saccharomytacea and Sporidiobolacea were more prevalent, while in spring and fall Trichocomacea (overall, the most prevalent family isolated throughout this study) were the most abundant taxa isolated at these depths as well as at deeper sampling sites. Our results highlight the dynamic nature of the culturable coral mycobiome and its sensitivity to environmental conditions and coral health. Full article

(This article belongs to the Special Issue The Human Epoch: Cnidarians Holobiont Responses from Physiology to Epigenetic)

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16 pages, 1971 KiB

Open AccessArticle

Coral Productivity Is Co-Limited by Bicarbonate and Ammonium Availability

by Stephane Roberty, Eric Béraud, Renaud Grover and Christine Ferrier-Pagès

Microorganisms 2020, 8(5), 640; https://doi.org/10.3390/microorganisms8050640 - 28 Apr 2020

Cited by 17 | Viewed by 3217

Abstract

The nitrogen environment and nitrogen status of reef-building coral endosymbionts is one of the important factors determining the optimal assimilation of phototrophic carbon and hence the growth of the holobiont. However, the impact of inorganic nutrient availability on the photosynthesis and physiological state [...] Read more.

The nitrogen environment and nitrogen status of reef-building coral endosymbionts is one of the important factors determining the optimal assimilation of phototrophic carbon and hence the growth of the holobiont. However, the impact of inorganic nutrient availability on the photosynthesis and physiological state of the coral holobiont is partly understood. This study aimed to determine if photosynthesis of the endosymbionts associated with the coral Stylophora pistillata and the overall growth of the holobiont were limited by the availability of dissolved inorganic carbon and nitrogen in seawater. For this purpose, colonies were incubated in absence or presence of 4 µM ammonium and/or 6 mM bicarbonate. Photosynthetic performances, pigments content, endosymbionts density and growth rate of the coral colonies were monitored for 3 weeks. Positive effects were observed on coral physiology with the supplementation of one or the other nutrient, but the most important changes were observed when both nutrients were provided. The increased availability of DIC and NH₄⁺ significantly improved the photosynthetic efficiency and capacity of endosymbionts, in turn enhancing the host calcification rate. Overall, these results suggest that in hospite symbionts are co-limited by nitrogen and carbon availability for an optimal photosynthesis. Full article

(This article belongs to the Special Issue The Human Epoch: Cnidarians Holobiont Responses from Physiology to Epigenetic)

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16 pages, 2884 KiB

Open AccessArticle

Effects of Light Pollution on the Early Life Stages of the Most Abundant Northern Red Sea Coral

by Raz Tamir, Gal Eyal, Itay Cohen and Yossi Loya

Microorganisms 2020, 8(2), 193; https://doi.org/10.3390/microorganisms8020193 - 31 Jan 2020

Cited by 20 | Viewed by 5105

Abstract

The growth in human population along coastal areas is exposing marine environments to increasing anthropogenic light sources. Despite the potential effects of this modern phenomenon, very few studies have examined its implications for corals. Here, we present a long-term study of coral early [...] Read more.

The growth in human population along coastal areas is exposing marine environments to increasing anthropogenic light sources. Despite the potential effects of this modern phenomenon, very few studies have examined its implications for corals. Here, we present a long-term study of coral early life stages under light pollution conditions at night. Coral larvae were collected from Stylophora pistillata colonies, and then settled and grown under experimental conditions of two different common city lighting methods (fluorescent or LED). Effects of the artificial lighting on the coral settlement success, survivorship, growth rate, photosynthetic efficiency, and calcification rate were examined over a period of one year. The control exhibited ~30% higher settlement success compared to the two light treatments, while under the light treatments corals showed higher survivorship, growth, and calcification rates. In addition, an indication of damage to the photosynthetic system was found in the light-polluted corals, which was reflected in their photosynthesis efficiency parameters: i.e., lower maximum light utilization coefficient (α), lower maximum potential photosynthetic rate (P_max), and lower photosynthetic maximal quantum yield (F_v/F_m). Our findings provide evidence of the potential adverse effects of artificial lighting methods on the natural environment of coral reefs. We conclude that the use of the LED lighting method has high interference potential for the early life stages of corals. Full article

(This article belongs to the Special Issue The Human Epoch: Cnidarians Holobiont Responses from Physiology to Epigenetic)

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18 pages, 4666 KiB

Open AccessArticle

The Effect of Thermal Stress on the Bacterial Microbiome of Exaiptasia diaphana

by Leon M. Hartman, Madeleine J. H. van Oppen and Linda L. Blackall

Microorganisms 2020, 8(1), 20; https://doi.org/10.3390/microorganisms8010020 - 20 Dec 2019

Cited by 15 | Viewed by 4189

Abstract

Coral bleaching linked to climate change has generated interest in the response of coral’s bacterial microbiome to thermal stress. The sea anemone, Exaiptasia diaphana, is a popular coral model, but the response of its bacteria to thermal stress has been barely explored. [...] Read more.

Coral bleaching linked to climate change has generated interest in the response of coral’s bacterial microbiome to thermal stress. The sea anemone, Exaiptasia diaphana, is a popular coral model, but the response of its bacteria to thermal stress has been barely explored. To address this, we compared the bacterial communities of Great Barrier Reef (GBR) E. diaphana maintained at 26 °C or exposed to increasing temperature (26–33 °C) over two weeks. Communities were analyzed by metabarcoding of the bacterial 16S rRNA gene. Bleaching and Symbiodiniaceae health were assessed by Symbiodiniaceae cell density and dark-adapted quantum yield (F_v/F_m), respectively. Significant bleaching and reductions in F_v/F_m occurred in the heat-treated anemones above 29 °C. Overall declines in bacterial alpha diversity in all anemones were also observed. Signs of bacterial change emerged above 31 °C. Some initial outcomes may have been influenced by relocation or starvation, but collectively, the bacterial community and taxa-level data suggested that heat was the primary driver of change above 32 °C. Six bacterial indicator species were identified as potential biomarkers for thermal stress. We conclude that the bacterial microbiome of GBR E. diaphana is generally stable until a thermal threshold is surpassed, after which significant changes occur. Full article

(This article belongs to the Special Issue The Human Epoch: Cnidarians Holobiont Responses from Physiology to Epigenetic)

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