Phylogenetic analysis of apicomplexan parasites infecting commercially valuable species from the North-East Atlantic reveals high levels of diversity and insights into the evolution of the group
Abstract:BackgroundThe Apicomplexa from aquatic environments are understudied relative to their terrestrial counterparts, and the seminal work assessing the phylogenetic relations of fish-infecting lineages is mostly based on freshwater hosts. The taxonomic uncertainty of some apicomplexan groups, such as the coccidia, is high and many genera were recently shown to be paraphyletic, questioning the value of strict morphological and ecological traits for parasite classification. Here, we surveyed the genetic diversity of… Show more
“…A novel Apicomplexa, parasitic alveolate specific to the Scomber japonicus fish species was discovered which had a high prevalence in all body sites, particularly the gill and pyloric ceca. Relatively little is known about the genetics and evolution of Apicomplexa parasites, but several coccidia, including Eimeria , Goussia , and Calyptospora , have been recently identified in various species of commercially important marine fish ( 24 ). Lastly, an important fish pathogen, Photobacterium damselae , was observed in high prevalence on GI, skin, and digesta communities and was associated with the summer months, which exhibit higher temperatures and low nutrients.…”
Changing ocean conditions driven by anthropogenic activities may have a negative impact on fisheries by increasing stress and disease. To understand how environment and host biology drives mucosal microbiomes in a marine fish, we surveyed five body sites (gill, skin, digesta, gastrointestinal tract [GI], and pyloric ceca) from 229 Pacific chub mackerel, Scomber japonicus, collected across 38 time points spanning 1 year from the Scripps Institution of Oceanography Pier (La Jolla, CA). Mucosal sites had unique microbial communities significantly different from the surrounding seawater and sediment communities with over 10 times more total diversity than seawater. The external surfaces of skin and gill were more similar to seawater, while digesta was more similar to sediment. Alpha and beta diversity of the skin and gill was explained by environmental and biological factors, specifically, sea surface temperature, chlorophyll a, and fish age, consistent with an exposure gradient relationship. We verified that seasonal microbial changes were not confounded by regional migration of chub mackerel subpopulations by nanopore sequencing a 14,769-bp region of the 16,568-bp mitochondria across all temporal fish specimens. A cosmopolitan pathogen, Photobacterium damselae, was prevalent across multiple body sites all year but highest in the skin, GI, and digesta between June and September, when the ocean is warmest. The longitudinal fish microbiome study evaluates the extent to which the environment and host biology drives mucosal microbial ecology and establishes a baseline for long-term surveys linking environment stressors to mucosal health of wild marine fish.
IMPORTANCE Pacific chub mackerel, Scomber japonicus, are one of the largest and most economically important fisheries in the world. The fish is harvested for both human consumption and fish meal. Changing ocean conditions driven by anthropogenic stressors like climate change may negatively impact fisheries. One mechanism for this is through disease. As waters warm and chemistry changes, the microbial communities associated with fish may change. In this study, we performed a holistic analysis of all mucosal sites on the fish over a 1-year time series to explore seasonal variation and to understand the environmental drivers of the microbiome. Understanding seasonality in the fish microbiome is also applicable to aquaculture production for producers to better understand and predict when disease outbreaks may occur based on changing environmental conditions in the ocean.
“…A novel Apicomplexa, parasitic alveolate specific to the Scomber japonicus fish species was discovered which had a high prevalence in all body sites, particularly the gill and pyloric ceca. Relatively little is known about the genetics and evolution of Apicomplexa parasites, but several coccidia, including Eimeria , Goussia , and Calyptospora , have been recently identified in various species of commercially important marine fish ( 24 ). Lastly, an important fish pathogen, Photobacterium damselae , was observed in high prevalence on GI, skin, and digesta communities and was associated with the summer months, which exhibit higher temperatures and low nutrients.…”
Changing ocean conditions driven by anthropogenic activities may have a negative impact on fisheries by increasing stress and disease. To understand how environment and host biology drives mucosal microbiomes in a marine fish, we surveyed five body sites (gill, skin, digesta, gastrointestinal tract [GI], and pyloric ceca) from 229 Pacific chub mackerel, Scomber japonicus, collected across 38 time points spanning 1 year from the Scripps Institution of Oceanography Pier (La Jolla, CA). Mucosal sites had unique microbial communities significantly different from the surrounding seawater and sediment communities with over 10 times more total diversity than seawater. The external surfaces of skin and gill were more similar to seawater, while digesta was more similar to sediment. Alpha and beta diversity of the skin and gill was explained by environmental and biological factors, specifically, sea surface temperature, chlorophyll a, and fish age, consistent with an exposure gradient relationship. We verified that seasonal microbial changes were not confounded by regional migration of chub mackerel subpopulations by nanopore sequencing a 14,769-bp region of the 16,568-bp mitochondria across all temporal fish specimens. A cosmopolitan pathogen, Photobacterium damselae, was prevalent across multiple body sites all year but highest in the skin, GI, and digesta between June and September, when the ocean is warmest. The longitudinal fish microbiome study evaluates the extent to which the environment and host biology drives mucosal microbial ecology and establishes a baseline for long-term surveys linking environment stressors to mucosal health of wild marine fish.
IMPORTANCE Pacific chub mackerel, Scomber japonicus, are one of the largest and most economically important fisheries in the world. The fish is harvested for both human consumption and fish meal. Changing ocean conditions driven by anthropogenic stressors like climate change may negatively impact fisheries. One mechanism for this is through disease. As waters warm and chemistry changes, the microbial communities associated with fish may change. In this study, we performed a holistic analysis of all mucosal sites on the fish over a 1-year time series to explore seasonal variation and to understand the environmental drivers of the microbiome. Understanding seasonality in the fish microbiome is also applicable to aquaculture production for producers to better understand and predict when disease outbreaks may occur based on changing environmental conditions in the ocean.
“…The Haemohormidium -like parasite was basal to a major monophyletic clade containing species of coccidia, a finding comparable to that of Renoux et al (2017) . Furthermore, amplicons retrieved in this study and in Renoux et al (2017) formed a monophyletic clade with that of apicomplexans of unknown identity retrieved during a molecular survey from tissues of the liver of Solea senegalensis ( MF468328 ) and the heart of Pagrus caeruleostictus ( MF468323 ), both species of fish collected from the Northeast Atlantic (see Xavier et al, 2018 ). Fig.…”
Section: Resultsmentioning
confidence: 63%
“…For the phylogenetic analysis sequences generated of the Haemohormidium -like parasite from the different species of damselfish and from the different sites were compared. Comparative sequences of coccidia (with reference to the findings of Renoux et al, 2017 ) with Adelina dimidiata (GenBank: DQ096835 ) as outgroup (following Barta et al, 2012 ; Xavier et al, 2018 ), were downloaded from GenBank and aligned to the sequences generated within this study. Sequences were aligned using the Clustal W alignment tool ( Thompson et al, 1994 ) implemented in Geneious Ver.…”
Section: Methodsmentioning
confidence: 99%
“…The alignment consisted of 43 sequences and was 1100 nt in length, with the exception of six sequences ( MF468290 , MF468291 , MF468292 , MF468293 , MF468323 , MF468328 ) being ∼500 nt. These shorter sequences were included as they represent species of coccidia recently isolated from marine fish hosts by Xavier et al (2018) , two of these falling with a Haemohormidium -like parasite isolated by Renoux et al (2017) (see Xavier et al, 2018 ). To infer phylogenetic relationships of the aligned dataset a Bayesian inference (BI) method was used.…”
Coral reefs harbor the greatest biodiversity per unit area of any ecosystem on earth. While parasites constitute the majority of this biodiversity, they remain poorly studied due to the cryptic nature of many parasites and the lack of appropriate training among coral reef ecologists. Damselfishes (Pomacentridae) are among the most abundant and diverse fishes on coral reefs. In a recent study of blood parasites of Caribbean reef fishes, the first ever apicomplexan blood parasites discovered in damselfishes were reported for members of the genus Stegastes. While these blood parasites were characterized as “Haemohormidium-like”, they appear to be distinct from any other known apicomplexan. In this study, we examined host associations, geographic distributions, and provide further insights on the phylogenetic affiliation of this parasite. A combination of morphological characteristics and 18S rDNA sequences suggest that this parasite may be the same species at multiple sites and occurs from the southern to the northern extreme of the eastern Caribbean, although it appears rare in the north. At present it appears to be limited to members of the genus Stegastes and infects all life history stages. It is most common in benthophagous species that occur in high population densities and appears basal to a major monophyletic clade containing species of coccidia, distinct from the Piroplasmida, the order to which Haemohormidium spp. have been assigned. These findings suggest a possible fecal-oral mode of transmission.
“…The SSR rDNA‐based phylogeny obtained in the present study returned an arrangement similar to that found in previous studies, with the clade composed by species of the genus Goussia and Eimeria with marked polyphyletic (Jirku et al, ; Xavier et al, ). The findings of the Bayesian inference, together with the divergences observed in the morphology of the oocysts and sporocysts of Goussia guamaensis n. sp.…”
Ninety‐seven specimens of spotfin hatchetfish, Thoracocharax stellatus, an ornamental freshwater species from the Amazon basin, were captured in the basin of the Guamá River in the municipality of Belém, in northern Brazil, and analysed for coccidiosis infection. Overall, 26 of the specimens were infected by apicomplexan parasites of the genus Goussia, with unsporulated forms being found in the gastric epithelium and sporulated forms in the intestinal lumen. The spheroid oocysts (mean diameter: 13.2 ± 1.7 μm) have four elliptical sporocysts. A partial sequence of the SSU rDNA of the new species was obtained, which contained 1,121 base pairs, with 43.8% guanine + cytosine (G + C), and the bases distributed as follows: A = 28.1%, C = 18.3%, G = 25.5% and T = 28.1%. The combined analysis of the morphometric and phylogenetic evidence confirmed that the specimens represented the genus Goussia and were allocated to a new species, Goussia guamaensis n. sp., which is described here.
scite is a Brooklyn-based organization that helps researchers better discover and understand research articles through Smart Citations–citations that display the context of the citation and describe whether the article provides supporting or contrasting evidence. scite is used by students and researchers from around the world and is funded in part by the National Science Foundation and the National Institute on Drug Abuse of the National Institutes of Health.
