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草皮海藻对珊瑚微生物群落结构与功能的影响:以涠洲岛澄黄滨珊瑚为例
廖芝衡, 余克服, 俞小鹏, 陈飚, 徐轶肖, 胡宝清, 姚秋翠, 许莉佳, 王永智
海洋学研究 ›› 2026, Vol. 44 ›› Issue (3) : 115-128.
PDF(4778 KB)
PDF(4778 KB)
草皮海藻对珊瑚微生物群落结构与功能的影响:以涠洲岛澄黄滨珊瑚为例
Effects of turf algae on the structure and function of coral microbial communities: a case study of Porites lutea from Weizhou Island
草皮海藻对珊瑚生长的不利影响日益严重,然而草皮海藻竞争作用影响珊瑚健康的微生物机制尚不明确。本研究基于高通量测序,分析了涠洲岛珊瑚礁区草皮海藻接触对澄黄滨珊瑚(Porites lutea)细菌群落多样性、组成与基因功能的影响。结果显示,草皮海藻细菌群落α多样性显著高于健康珊瑚,与草皮海藻接触会显著增加珊瑚细菌群落α多样性,并促使珊瑚细菌群落组成趋同于草皮海藻。差异性分析显示,相较于健康珊瑚,接触草皮海藻的珊瑚组织中假交替单胞菌属(Pseudoalteromonas)、内共生单胞菌属(Endozoicomonas)、鲁杰氏菌属(Ruegeria)及罗尔斯通氏菌属(Ralstonia)等优势共生有益菌相对丰度显著下降,而伍斯氏菌属(Woeseia)等潜在致病菌及部分致病性未知细菌的相对丰度则显著上升。此外,基于 PICRUSt2 预测的 KEGG 二级功能水平分析显示,草皮海藻接触分别造成珊瑚细菌能量代谢功能基因相对丰度显著上升、脂质代谢功能基因相对丰度显著下降。综上所述,草皮海藻接触促使珊瑚细菌群落多样性趋同于草皮海藻,减少珊瑚共生有益菌丰度、增加机会性病原体丰度,并加剧珊瑚细菌能量代谢、减少能量代谢底物来源,这些改变共同构成了草皮海藻影响珊瑚健康的潜在微生物机制。
The deleterious effects of turf algae overgrowth on coral performance have intensified across coral reef ecosystems; nevertheless, the microbial pathways mediating coral health deterioration driven by competitive turf algae interactions remain poorly characterized. Using 16S rRNA gene high-throughput amplicon sequencing, the present work explored how physical contact with turf algae alters the bacterial community diversity, taxonomic composition, and functional gene profiles of Porites lutea colonies at Weizhou Island coral reefs. Our findings showed that turf algae-associated bacterial communities exhibited substantially higher α-diversity than those colonizing healthy corals. Physical turf algae exposure significantly boosted the α-diversity of coral microbiomes and triggered taxonomic convergence between coral bacterial assemblages and turf algae microbiotas. Differential abundance testing illustrated that relative abundances of core coral symbiotic genera—including Pseudoalteromonas, Endozoicomonas, Ruegeria, and Ralstonia—were markedly depleted in coral tissues exposed to turf algae relative to healthy counterparts. In contrast, the putative pathogen Woeseia, alongside multiple uncharacterized bacterial taxa with undetermined pathogenic potential, underwent dramatic enrichment. Additionally, PICRUSt2-based functional prediction at the KEGG secondary pathway tier revealed that turf algae contact triggered significant upregulation of genes linked to energy metabolism and concurrent downregulation of lipid metabolism within coral bacterial consortia. Synthesizing these observations, physical turf algae contact remodels coral microbiomes to resemble turf algae-associated microbial assemblages: this contact suppresses populations of coral symbiotic beneficial taxa while enriching opportunistic pathogens, elevates overall bacterial energy metabolic capacity, and reduces lipid pools serving as key energy substrates. Such community and functional reorganizations may constitute the core microbial mechanisms through which turf algae competition compromises coral physiological fitness.
草皮海藻 / 澄黄滨珊瑚 / 接触 / 竞争作用 / 细菌多样性 / 基因功能 / 涠洲岛
turf algae / Porites lutea / contact / competitive interaction / bacterial diversity / gene function / Weizhou Island
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Coral reefs are increasingly threatened by various types of disturbances, and their recovery is challenged by accelerating, human-induced environmental changes. Recurrent disturbances reduce the pool of mature adult colonies of reef-building corals and undermine post-disturbance recovery from newly settled recruits. Using a long-term interannual data set, we show that coral assemblages on the reef slope of Moorea, French Polynesia, have maintained a high capacity to recover despite a unique frequency of large-scale disturbances which, since the 1990s, have caused catastrophic declines in coral cover and abundance. In 2014, only four years after one of the most extreme cases of coral decline documented, abundance of juvenile and adult colonies had regained or exceeded predisturbance levels, and no phase-shift to macroalgal dominance was recorded. This rapid recovery has been achieved despite constantly low coral recruitment rates, suggesting a high post-disturbance survivorship of recruits. However, taxonomic differences in coral susceptibility to disturbances and contrasting recovery trajectories have resulted in changes in the relative composition of species. In the present context of global coral reef decline, our study establishes a new benchmark for the capacity of certain benthic reef communities to sustain and recover their coral cover from repeated, intense disturbances.
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The use of standardised classifications, or operational definitions, is essential if different researchers are to measure and compare similar entities. In the marine realm, algal 'turfs' are increasingly reported to be globally expanding at the expense of kelps and canopy-forming algae. However, ecological research about the underlying drivers of this shift is limited by a vague and inconsistent definition of what exactly a turf is. In order to stimulate more effective descriptions of 'turfs' and facilitate communication of research outcomes and comparisons across studies, we reviewed the use of the term turf in ecological studies of temperate coasts and coral reefs and (1) identified the main types and distribution of algal assemblages known as 'turfs', (2) examined the descriptions of turfs so that we may recognise some general characteristics, including those contingent on environmental conditions; and (3) offered character descriptions that could improve communication and comparisons. These descriptors centre on reporting information on the morphology, height, density of thalli, the amount of sediment trapped in turfs and a description of the area covered by turfs, including their patchiness and persistence. Our review recognised these as common attributes that could be usefully described across a wide range of circumstances and provide insights into the ecology of turfs and their interactions with other assemblages in a community. The use of common descriptors would provide the term 'turf' with greater scientific value.
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罗海业. 南海中北部珊瑚礁区草皮海藻分布特征及其对石珊瑚的潜在影响[D]. 南宁: 广西大学, 2019.
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The increased release of dissolved organic matter (DOM) by algae has been associated with the fast but inefficient growth of opportunistic microbial pathogens and the ongoing degradation of coral reefs. Turf algae (consortia of microalgae and macroalgae commonly including cyanobacteria) dominate benthic communities on many reefs worldwide. Opposite to other reef algae that predominantly release DOM during the day, turf algae containing cyanobacteria may additionally release large amounts of DOM at night. However, this night-DOM release and its potential contribution to the microbialization of reefs remains to be investigated.We first tested the occurrence of hypoxic conditions at the turf algae-water interface, as a lack of oxygen will facilitate the production and release of fermentation intermediates as night-time DOM. Second, the dissolved organic carbon (DOC) release by turf algae was quantified during day time and nighttime, and the quality of day and night exudates as food for bacterioplankton was tested. Finally, DOC release rates of turf algae were combined with estimates of DOC release based on benthic community composition in 1973 and 2013 to explore how changes in benthic community composition affected the contribution of night-DOC to the reef-wide DOC production.A rapid shift from supersaturated to hypoxic conditions at the turf algae-water interface occurred immediately after the onset of darkness, resulting in night-DOC release rates similar to those during daytime. Bioassays revealed major differences in the quality between day and night exudates: Night-DOC was utilized by bacterioplankton two times faster than day-DOC, but yielded a four times lower growth efficiency. Changes in benthic community composition were estimated to have resulted in a doubling of DOC release since 1973, due to an increasing abundance of benthic cyanobacterial mats (BCMs), with night-DOC release by BCMs and turf algae accounting for >50% of the total release over a diurnal cycle.Night-DOC released by BCMs and turf algae is likely an important driver in the microbialization of reefs by stimulating microbial respiration at the expense of energy and nutrient transfer to higher trophic levels via the microbial loop, thereby threatening the productivity and biodiversity of these unique ecosystems. Read the free Plain Language Summary for this article on the Journal blog.© 2022 The Authors. Functional Ecology published by John Wiley & Sons Ltd on behalf of British Ecological Society.
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Coral reefs are in dramatic global decline, with seaweeds commonly replacing corals. It is unclear, however, whether seaweeds harm corals directly or colonize opportunistically following their decline and then suppress coral recruitment. In the Caribbean and tropical Pacific, we show that, when protected from herbivores, approximately 40 to 70% of common seaweeds cause bleaching and death of coral tissue when in direct contact. For seaweeds that harmed coral tissues, their lipid-soluble extracts also produced rapid bleaching. Coral bleaching and mortality was limited to areas of direct contact with seaweeds or their extracts. These patterns suggest that allelopathic seaweed-coral interactions can be important on reefs lacking herbivore control of seaweeds, and that these interactions involve lipid-soluble metabolites transferred via direct contact. Seaweeds were rapidly consumed when placed on a Pacific reef protected from fishing but were left intact or consumed at slower rates on an adjacent fished reef, indicating that herbivory will suppress seaweeds and lower frequency of allelopathic damage to corals if reefs retain intact food webs. With continued removal of herbivores from coral reefs, seaweeds are becoming more common. This occurrence will lead to increasing frequency of seaweed-coral contacts, increasing allelopathic suppression of remaining corals, and continuing decline of reef corals.
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Populations of Acropora palmata and Orbicella faveolata, two important reef-building corals, have declined precipitously across the Caribbean region since at least the 1970s. Recruitment failure may be limiting population recovery, possibly due to lack of suitable settlement habitat. Here, we examine the effects of algal turfs and algal turfs + sediment, two widely abundant substrate types across the Florida Keys, on the settlement of these two ecologically-important species. We show that sediment significantly impedes coral settlement, reducing settlement 10- and 13-fold for A. palmata and O. faveolata, respectively, compared to turf algae alone. This result is corroborated by our field survey data that showed a strong, negative relationship between the abundance of turf + sediment and the abundance of juvenile corals. Turf algae alone did not reduce coral settlement. Our results suggest that sediment-laden turf algae are detrimental to settling corals, but that turf algae alone may be relatively benign.Copyright © 2019 Elsevier Ltd. All rights reserved.
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The coral reef benthos is primarily colonized by corals and algae, which are often in direct competition with one another for space. Numerous studies have shown that coral-associated Bacteria are different from the surrounding seawater and are at least partially species specific (i.e. the same bacterial species on the same coral species). Here we extend these microbial studies to four of the major ecological functional groups of algae found on coral reefs: upright and encrusting calcifying algae, fleshy algae, and turf algae, and compare the results to the communities found on the reef-building coral Montastraea annularis. It was found using 16S rDNA tag pyrosequencing that the different algal genera harbour characteristic bacterial communities, and these communities were generally more diverse than those found on corals. While the majority of coral-associated Bacteria were related to known heterotrophs, primarily consuming carbon-rich coral mucus, algal-associated communities harboured a high percentage of autotrophs. The majority of algal-associated autotrophic Bacteria were Cyanobacteria and may be important for nitrogen cycling on the algae. There was also a rich diversity of photosynthetic eukaryotes associated with the algae, including protists, diatoms, and other groups of microalgae. Together, these observations support the hypothesis that coral reefs are a vast landscape of distinctive microbial communities and extend the holobiont concept to benthic algae.© 2011 Society for Applied Microbiology and Blackwell Publishing Ltd.
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Microbes influence ecological processes, including the dynamics and health of macro-organisms and their interactions with other species. In coral reefs, microbes mediate negative effects of algae on corals when corals are in contact with algae. However, it is unknown whether these effects extend to larger spatial scales, such as at sites with high algal densities. We investigated how local algal contact and site-level macroalgal cover influenced coral microbial communities in a field study at two islands in French Polynesia, Mo'orea and Mangareva. At 5 sites at each island, we sampled prokaryotic microbial communities (microbiomes) associated with corals, macroalgae, turf algae and water, with coral samples taken from individuals that were isolated from or in contact with turf or macroalgae. Algal contact and macroalgal cover had antagonistic effects on coral microbiome alpha and beta diversity. Additionally, coral microbiomes shifted and became more similar to macroalgal microbiomes at sites with high macroalgal cover and with algal contact, although the microbial taxa that changed varied by island. Our results indicate that coral microbiomes can be affected by algae outside of the coral's immediate vicinity, and local- and site-level effects of algae can obscure each other's effects when both scales are not considered.
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Most studies of stressors focus on the response of traditionally classified organisms via effects on growth, mortality or physiology; however, most species have microbial associates that may mediate the response of a host to the stressor. Additionally, species rarely experience one stressor alone, but instead are influenced by multiple, potentially interacting stressors. We evaluated how coral microbiomes responded to two biotic stressors: the vermetid gastropod, Ceraesignum maximum, and algal turfs, both of which have previously been shown to decrease coral growth, survival and photophysiology. We collected coral mucus from massive Porites colonies in the presence versus absence of both algae and vermetids and sequenced the 16S rRNA gene to characterize the coral surface microbial communities. The presence of algae increased the alpha diversity of the coral microbial community, likely by increasing the relative abundance of rare members of the community. Algae also reduced beta diversity, which we hypothesized was due to algae homogenizing the physical environment. In contrast, vermetids had only small effects on microbial communities, even though vermetids have deleterious effects on coral growth. We previously hypothesized that vermetids would exacerbate algal effects on microbes, but we failed to detect an interaction between vermetids and algae on the coral's microbiome, except for one family, Fusobacteriaceae, which was most abundant in the presence of both stressors. We suggest that algae can affect corals through their effects on microbes, whereas vermetids primarily affect the host directly; these complementary effects may limit the extent to which stressors can interact.
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Viruses, microbes, and host macroorganisms form ecological units called holobionts. Here, a combination of metagenomic sequencing, metabolomic profiling, and epifluorescence microscopy was used to investigate how the different components of the holobiont including bacteria, viruses, and their associated metabolites mediate ecological interactions between corals and turf algae. The data demonstrate that there was a microbial assemblage unique to the coral-turf algae interface displaying higher microbial abundances and larger microbial cells. This was consistent with previous studies showing that turf algae exudates feed interface and coral-associated microbial communities, often at the detriment of the coral. Further supporting this hypothesis, when the metabolites were assigned a nominal oxidation state of carbon (NOSC), we found that the turf algal metabolites were significantly more reduced (i.e., have higher potential energy) compared to the corals and interfaces. The algae feeding hypothesis was further supported when the ecological outcomes of interactions (e.g., whether coral was winning or losing) were considered. For example, coral holobionts losing the competition with turf algae had higher Bacteroidetes-to-Firmicutes ratios and an elevated abundance of genes involved in bacterial growth and division. These changes were similar to trends observed in the obese human gut microbiome, where overfeeding of the microbiome creates a dysbiosis detrimental to the long-term health of the metazoan host. Together these results show that there are specific biogeochemical changes at coral-turf algal interfaces that predict the competitive outcomes between holobionts and are consistent with algal exudates feeding coral-associated microbes.Copyright © 2020 the Author(s). Published by PNAS.
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Recent work has shown that hydrophilic and hydrophobic organic matter (OM) from algae disrupts the function of the coral holobiont and promotes the invasion of opportunistic pathogens, leading to coral morbidity and mortality. Here we refer to these dynamics as the (3)DAM [dissolved organic matter (DOM), direct contact, disease, algae and microbes] model. There is considerable complexity in coral-algae interactions; turf algae and macroalgae promote heterotrophic microbial overgrowth of coral, macroalgae also directly harm the corals via hydrophobic OM, whereas crustose coralline algae generally encourage benign microbial communities. In addition, complex flow patterns transport OM and pathogens from algae to downstream corals, and direct algal contact enhances their delivery. These invisible players (microbes, viruses, and OM) are important drivers of coral reefs because they have non-linear responses to disturbances and are the first to change in response to perturbations, providing near real-time trajectories for a coral reef, a vital metric for conservation and restoration.Copyright © 2012 Elsevier Ltd. All rights reserved.
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The inhibitory properties of the microbial community of the coral mucus from the Mediterranean coral Oculina patagonica were examined. Out of 156 different colony morphotypes that were isolated from the coral mucus, nine inhibited the growth of Vibrio shiloi, a species previously shown to be a pathogen of this coral. An isolate identified as Pseudoalteromonas sp. was the strongest inhibitor of V. shiloi. Several isolates, especially one identified as Roseobacter sp., also showed a broad spectrum of action against the coral pathogens Vibrio coralliilyticus and Thallassomonas loyana, plus nine other selected Gram-positive and Gram-negative bacteria. Inoculation of a previously established biofilm of the Roseobacter strain with V. shiloi led to a 5-log reduction in the viable count of the pathogen within 3 h, while inoculation of a Pseudoalteromonas biofilm led to complete loss of viability of V. shiloi after 3 h. These results support the concept of a probiotic effect on microbial communities associated with the coral holobiont.
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Stony corals, the engines and engineers of reef ecosystems, face unprecedented threats from anthropogenic environmental change. Corals are holobionts that comprise the cnidarian animal host and a diverse community of bacteria, archaea, viruses and eukaryotic microorganisms. Recent research shows that the bacterial microbiome has a pivotal role in coral biology. A healthy bacterial assemblage contributes to nutrient cycling and stress resilience, but pollution, overfishing and climate change can break down these symbiotic relationships, which results in disease, bleaching and, ultimately, coral death. Although progress has been made in characterizing the spatial-temporal diversity of bacteria, we are only beginning to appreciate their functional contribution. In this Review, we summarize the ecological and metabolic interactions between bacteria and other holobiont members, highlight the biotic and abiotic factors influencing the structure of bacterial communities and discuss the impact of climate change on these communities and their coral hosts. We emphasize how microbiome-based interventions can help to decipher key mechanisms underpinning coral health and promote reef resilience. Finally, we explore how recent technological developments may be harnessed to address some of the most pressing challenges in coral microbiology, providing a road map for future research in this field.© 2024. Springer Nature Limited.
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Increased seawater temperatures and nutrient loading are stressors that affect coral reefs and their microbiomes. In this study, filamentous algae were collected and exposed to different temperatures and nutrient concentrations through a laboratory experiment. Microbial DNA was extracted and analyzed using amplicon sequencing of the V3-V4 hypervariable region of the 16S rRNA gene. In total, 1 domain, 51 phyla, 131 classes, 335 orders, 549 families, and 1905 species were identified. Proteobacteria and Bacteroidota were the dominant taxa reported. Elevated seawater temperatures and nutrient enrichment impacted microbial communities associated with turf algae under laboratory culture. Bacterial species diversity and abundance differed under different temperature and nutrient conditions. Proteobacteria and Actinobacteria were abundant in lower-temperature conditions, while Desulfobacterota, Spirochaetota, and Firmicutes were abundant in higher-temperature conditions. Ruegeria was abundant in low-temperature conditions, whereas Vibrio abundance was low. Regarding nutrient conditions, Proteobacteria and Cyanobacteria were abundant under high-nutrient conditions, while Firmicutes and Desulfobacterota were abundant under ambient-nutrient conditions. The higher nutrient concentration increased the abundance of pathogenic bacteria, such as Vibrio and Photobacterium, while Pseudoalteromonas, which is beneficial for reefs, was present under ambient nutrient conditions. This study demonstrates that temperature and nutrient enrichment can shape microbial communities under laboratory conditions, providing an experimental setting for further studies of bacterial functions and metabolic processes in natural conditions under thermal and nutrient stresses.
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余克服, 蒋明星, 程志强, 等. 涠洲岛42年来海面温度变化及其对珊瑚礁的影响[J]. 应用生态学报, 2004, 15(3): 506-510.
涠洲岛位于南海珊瑚礁分布的北缘.温度是影响其珊瑚礁生态系统发育的重要因素.对器测温度分析发现,近42年来涠洲岛海面温度(SST)与全球气候变暖呈准同步变化趋势,存在3～4年与7～8年的变化周期,20世纪80年代后期以来,涠洲岛SST上升比较明显.其月平均最高SST的持续上升将使本区珊瑚生长处于一种非常敏感的边缘,加上人类活动(建筑取材、炼油、旅游、捕鱼、养殖等)对涠洲岛珊瑚礁的潜在不利影响,则可能导致珊瑚礁的退化.此外,在系统的野外调查基础上,描述了涠洲岛现代珊瑚礁的分布范围.
Weizhou Island (109°00'～109°15'E,21°00'～21°10'N) locates in the north coral reef distribution belt of the South China Sea.In such relatively high latitude area,sea surface temperature (SST) is an important factor affecting the development of coral reef ecosystem.Measurements of the latest 42 years' SST of Weizhou Island showed that with 3～4 years and 7～8 years fluctuating cycles,the SST almost had a synchronous increase with global warming,especially since the later 1980s.Overall,the coral reef of Weizhou Island could benefit from the SST warming,especially the cold months SST increase,because it's the north margin of tropical zone.But,the warming of the warmest month may be a thermal stress on the development of coral reef.It reaches the upper limits of coral reef development,and leads the coral reef bleaching.Mankind activities,including wide scale building,oil gas factory near the island,traveling,fishing and breeding,may be also the potential stresses on limiting the coral reef development.The combination of summer warming and mankind stress is possibly to destroy the coral reef ecosystem of Weizhou Island.Based on a detailed field investigation,the modern coral reef distribution map around Weizhou Island was described.
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Corals harbor diverse and abundant prokaryotic populations. Bacterial communities residing in the coral mucus layer may be either pathogenic or symbiotic. Some species may produce antibiotics as a method of controlling populations of competing microbial species. The present study characterizes cultivable Pseudoalteromonas sp. isolated from the mucus layer of different coral species from the northern Gulf of Eilat, Red Sea, Israel. Six mucus-associated Pseudoalteromonas spp. obtained from different coral species were screened for antibacterial activity against 23 tester strains. Five of the six Pseudoalteromonas strains demonstrated extracellular antibacterial activity against Gram-positive-but not Gram-negative-tester strains. Active substances secreted into the cell-free supernatant are heat-tolerant and inhibit growth of Bacillus cereus, Staphylococcus aureus, and of ten endogenous Gram-positive marine bacteria isolated from corals. The Pseudoalteromonas spp. isolated from Red sea corals aligned in a phylogenetic tree with previously isolated Pseudoalteromonas spp. of marine origin that demonstrated antimicrobial activity. These results suggest that coral mucus-associated Pseudoalteromonas may play a protective role in the coral holobiont's defense against potential Gram-positive coral pathogens.
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Endozoicomonas are prevalent, abundant bacterial associates of marine animals, including corals. Their role in holobiont health and functioning, however, remains poorly understood. To identify potential interactions within the coral holobiont, we characterized the novel isolate Endozoicomonas marisrubri sp. nov. 6c and assessed its transcriptomic and proteomic response to tissue extracts of its native host, the Red Sea coral Acropora humilis. We show that coral tissue extracts stimulated differential expression of genes putatively involved in symbiosis establishment via the modulation of the host immune response by E. marisrubri 6c, such as genes for flagellar assembly, ankyrins, ephrins, and serpins. Proteome analyses revealed that E. marisrubri 6c upregulated vitamin B1 and B6 biosynthesis and glycolytic processes in response to holobiont cues. Our results suggest that the priming of Endozoicomonas for a symbiotic lifestyle involves the modulation of host immunity and the exchange of essential metabolites with other holobiont members. Consequently, Endozoicomonas may play an important role in holobiont nutrient cycling and may therefore contribute to coral health, acclimatization, and adaptation.
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