Large-scale impact of the 2016 Marine Heatwave on the plankton-associated microbial communities of the Great Barrier Reef (Australia)

Doni, Lapo; Oliveri, Caterina; Lasa, Aide; Cesare, Andrea Di; Petrin, Sara; Martı́nez-Urtaza, Jaime; Coman, Frank; Richardson, Anthony J.; Vezzulli, Luigi

doi:10.1016/j.marpolbul.2023.114685

Cited by 12 publications

(11 citation statements)

References 62 publications

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“…This could reflect their fastidious nature, but the success of the two northernmost Atlantic populations harboring inoviruses contrasting with the unsuccessful lineages that lacked them signals alternatives are possible: that inoviruses may confer advantages in some as yet undefined context. For example, shed inovirus virions contribute to biofilm matrix ( 65 ) thereby promoting virulence and antimicrobial resistance but also potentially enhancing survival during long-distance movement on particles ( 53 , 55 , 66 – 68 ). Shed inoviruses can mislead human immune responses and decrease host ability to clear bacterial infections, thereby enhancing virulence ( 69 ).…”

Section: Discussionmentioning

confidence: 99%

Inoviridae prophage and bacterial host dynamics during diversification, succession, and Atlantic invasion of Pacific-native Vibrio parahaemolyticus

Foxall,

Means,

Marcinkiewicz

et al. 2024

mBio

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The epidemiology of Vibrio parahaemolyticus , the leading cause of seafood-borne bacterial gastroenteritis of humans worldwide, dramatically changed in the United States following the establishment of a Pacific-native lineage called sequence type (ST) 36 in the Atlantic. In this study, we used phylogeography based on traceback to environmental source locations and comparative genomics to identify features that promoted evolution, dispersal, and competitive dominance of ST36. The major genomic differentiation and competitive success of ST36 were associated with a striking succession of filamentous prophage in the family Inoviridae (inoviruses), including loss of an inovirus prophage that had been maintained for decades in the endemic north Pacific population. Subsequently, at least five distinct progenitors arising from this diversification translocated from the Pacific into the Atlantic and established four geographically defined clonal subpopulations with remarkably low migration or mixing. Founders of two prevailing Atlantic subpopulations each acquired new stable and diagnostic inoviruses while other subpopulations that apparently declined did not. Broader surveys indicate inoviruses are common and active among the global population of V. parahaemolyticus , and though inovirus replacements, such as in ST36, appear to be infrequent, they are notable in pathogenic lineages that dispersed. IMPORTANCE An understanding of the processes that contribute to the emergence of pathogens from environmental reservoirs is critical as changing climate precipitates pathogen evolution and population expansion. Phylogeographic analysis of Vibrio parahaemolyticus hosts combined with the analysis of their Inoviridae phage resolved ambiguities of diversification dynamics which preceded successful Atlantic invasion by the epidemiologically predominant ST36 lineage. It has been established experimentally that filamentous phage can limit host recombination, but here, we show that phage loss is linked to rapid bacterial host diversification during epidemic spread in natural ecosystems alluding to a potential role for ubiquitous inoviruses in the adaptability of pathogens. This work paves the way for functional analyses to define the contribution of inoviruses in the evolutionary dynamics of environmentally transmitted pathogens.

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Section: Discussionmentioning

confidence: 99%

Inoviridae prophage and bacterial host dynamics during diversification, succession, and Atlantic invasion of Pacific-native Vibrio parahaemolyticus

Foxall,

Means,

Marcinkiewicz

et al. 2024

mBio

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show abstract

“…5) emphasizes that inoviruses may confer key advantages in some ecological contexts. Shed inovirus particles contribute to biofilm matrix (63) and prophage can regulate biofilm production which not only confers enhanced virulence through immune evasion and antimicrobial resistance, but also could contribute to survival during long distance movement through attachment to marine particles and plankton (52,54,(64)(65)(66). Variable content in inoviruses is also linked to antipredation (17,67) and virulence (22,27,39).…”

Section: Discussionmentioning

confidence: 99%

Inoviridaeprophage and bacterial host dynamics during diversification, succession and Atlantic invasion of Pacific-nativeVibrio parahaemolyticus

Means

Marcinkiewicz

Foxall

et al. 2023

Preprint

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The epidemiology ofVibrio parahaemolyticus, the leading cause of seafood-borne gastroenteritis world-wide, dramatically changed in the United States following the translocation and establishment of a Pacific lineage ofV. parahaemolyticus, sequence type (ST) 36, into the Atlantic. In this study we used phylogeography based on traceback locations and comparative genomics to identify features that promoted evolution, dispersal, and competitive dominance of ST36. This revealed a striking shuffling of filamentous prophage in the familyInoviridae(inoviruses), including loss of a prophage that had been maintained for decades, accompanied modern diversification and competitive replacement of the endemic north Pacific population. Subsequently, at least five distinct progenitors arising from this diversification translocated from the Pacific into the Atlantic and established four geographically defined clonal subpopulations with remarkably low migration or mixing. Founders of two prevailing Atlantic subpopulations each acquired new diagnostic inoviruses while other subpopulations that apparently declined did not. Broader surveys indicate inoviruses are common and active among the global population ofV. parahaemolyticusand though parallel inovirus replacements, such as in ST36, appear infrequent, they are notable in pathogenic lineages that dispersed. Importance: An understanding of the processes that contribute to emergence of pathogens from environmental reservoirs is critical as changing climate precipitates pathogen evolution and population expansion. Phylogeographic analysis ofVibrio parahaemolyticushosts combined with analysis of theirInoviridaephage resolved ambiguities of diversification dynamics which preceded successful Atlantic invasion by the epidemiologically predominant ST36 lineage. It has been established experimentally that filamentous phage can limit host recombination, but here we show that phage loss is linked to rapid bacterial host diversification during epidemic spread in natural ecosystems alluding to a potential role for ubiquitous inoviruses in the adaptability of pathogens. This work paves the way for functional analyses to define the contribution of inoviruses in the evolutionary dynamics of environmentally transmitted pathogens.

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“…climate warming) is well accepted across many terrestrial, freshwater and marine ecosystems [ 85 , 94 – 98 ], and acquisition of microbial pathogens from the environment has been documented in some food- and waterborne diseases [ 37 , 99 ]. For corals, there are many examples of putative microbial pathogens (isolated from diseased coral tissues) also being identified in the surrounding reef seawater, which often increase in their abundance and activity at elevated seawater temperatures [ 86 , 100 , 101 ]. The bacterial genus Vibrio sp.…”

Section: Experimental Validation Of Microbes That Predict Poor Reef H...mentioning

confidence: 99%

“…Another study identified a significant enrichment in Planctomycetota (lineages OM190 and CL500-3) and bacteria within genera Synechococcus and Vibrio during the marine heatwave on the GBR in April 2016, alongside an enrichment of Vibrio -derived virulence factors (i.e. metalloprotease genes vcpA, vcpB and vchA in V. coralliilyticus ) [ 101 ]. Though as the authors highlight, a link between large-scale changes observed in the plankton-associated microbial community and reef ecosystem health could not be established based on their observations [ 101 ], which warrants for robust experimental validation to gain a cause-and-effect understanding between the presence of potentially pathogenic water-born microorganisms and coral disease outbreaks.…”

Section: Experimental Validation Of Microbes That Predict Poor Reef H...mentioning

confidence: 99%

The road forward to incorporate seawater microbes in predictive reef monitoring

Terzin,

Laffy,

Robbins

et al. 2024

Environmental Microbiome

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Marine bacterioplankton underpin the health and function of coral reefs and respond in a rapid and sensitive manner to environmental changes that affect reef ecosystem stability. Numerous meta-omics surveys over recent years have documented persistent associations of opportunistic seawater microbial taxa, and their associated functions, with metrics of environmental stress and poor reef health (e.g. elevated temperature, nutrient loads and macroalgae cover). Through positive feedback mechanisms, disturbance-triggered heterotrophic activity of seawater microbes is hypothesised to drive keystone benthic organisms towards the limit of their resilience and translate into shifts in biogeochemical cycles which influence marine food webs, ultimately affecting entire reef ecosystems. However, despite nearly two decades of work in this space, a major limitation to using seawater microbes in reef monitoring is a lack of a unified and focused approach that would move beyond the indicator discovery phase and towards the development of rapid microbial indicator assays for (near) real-time reef management and decision-making. By reviewing the current state of knowledge, we provide a comprehensive framework (defined as five phases of research and innovation) to catalyse a shift from fundamental to applied research, allowing us to move from descriptive to predictive reef monitoring, and from reactive to proactive reef management.

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Large-scale impact of the 2016 Marine Heatwave on the plankton-associated microbial communities of the Great Barrier Reef (Australia)

Cited by 12 publications

References 62 publications

Inoviridae prophage and bacterial host dynamics during diversification, succession, and Atlantic invasion of Pacific-native Vibrio parahaemolyticus

Inoviridae prophage and bacterial host dynamics during diversification, succession, and Atlantic invasion of Pacific-native Vibrio parahaemolyticus

Inoviridaeprophage and bacterial host dynamics during diversification, succession and Atlantic invasion of Pacific-nativeVibrio parahaemolyticus

The road forward to incorporate seawater microbes in predictive reef monitoring

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