Intestinal microbiota composition in fishes is influenced by host ecology and environment

The digestive tracts of vertebrates are colonized by complex assemblages of micro-organisms, collectively called the gut microbiota. Recent studies have revealed important contributions of gut microbiota to vertebrate health and disease, stimulating intense interest in understanding how gut microbial communities are assembled and how they impact host fitness (Sekirov et al. 2010). Although all vertebrates harbour a gut microbiota, current information on microbiota composition and function has been derived primarily from mammals. Comparisons of different mammalian species have revealed intriguing associations between gut microbiota composition and host diet, anatomy and phylogeny (Ley et al. 2008b). However, mammals constitute <10% of all vertebrate species, and it remains unclear whether similar associations exist in more diverse and ancient vertebrate lineages such as fish. In this issue, Sullam et al. (2012) make an important contribution toward identifying factors determining gut microbiota composition in fishes. The authors conducted a detailed meta-analysis of 25 bacterial 16S rRNA gene sequence libraries derived from the intestines of different fish species. To provide a broader context for their analysis, they compared these data sets to a large collection of 16S rRNA gene sequence data sets from diverse free-living and host-associated bacterial communities. Their results suggest that variation in gut microbiota composition in fishes is strongly correlated with species habitat salinity, trophic level and possibly taxonomy. Comparison of data sets from fish intestines and other environments revealed that fish gut microbiota compositions are often similar to those of other animals and contain relatively few free-living environmental bacteria. These results suggest that the gut microbiota composition of fishes is not a simple reflection of the micro-organisms in their local habitat but may result from host-specific selective pressures within the gut (Bevins & Salzman 2011).     

土壤动物肠道微生物多样性研究进展

随着分子生物学技术方法的快速发展,动物肠道微生物已成为医学、动物生理学与微生物生态学等研究领域热点。土壤动物种类繁多,分布广泛,其作为陆地生态系统重要组分,是驱动生态系统功能的关键因子。土壤动物体内的微生物由于与宿主长期共存,在与宿主协同进化中形成了丰富多样的群落结构,能够影响土壤动物本身的健康,进而介导土壤动物生态功能的实现。近些年,土壤动物肠道微生物工作方兴未艾,日渐得到重视。总结了四个部分内容：1)首先总结了土壤动物肠道微生物多样性领域的研究现状,该领域年发文量逐年增长,且近十年增长快速。土壤模式生物肠道微生物多样性研究较多且更为深入。土壤动物肠道微生物多样性组成与驱动机制、共存机制及群落构建的理论研究是该领域前沿;2)进而展示了土壤动物肠道微生物多样性组成和研究方法,土壤动物肠道菌群组成以变形菌门、厚壁菌门、放线菌门和拟杆菌门为主。早期工作基于传统分离培养,近年来新一代测序技术推动了该领域发展;3)接着关注了土壤动物肠道微生物的生态学功能,总体上体现在肠道微生物能帮助宿主分解食物基质、参与营养利用、影响寿命和繁殖及提高宿主免疫能力,且其能够影响土壤动物的气体排放及介导其对生态系...     

Sediment processing by the surgeonfish Ctenochaetus striatus at Moorea, French Polynesia

The sediment-feeding surgeonfish Ctenochaetus striatus was found to reduce the sizes of ingested carbonaceous particles. The mean sizes of particles in stomach samples of the surgeonfish were smaller than those from areas where the fish were observed feeding. The particle sizes in the rectal contents of the fish were smaller than those in the stomach samples. The sediment-feeding activities of this and related surgeonfishes are likely to have a local impact on the particle-size distributions of sediments in reef and lagoon habitats. The assimilation efficiencies of the fish were estimated by the ash-ratio method to be 20% for total organic matter and 37% for nitrogen.     

Probiotic roles of Lactobacillus sp. in swine: insights from gut microbiota

The use of lactobacilli as probiotics in swine has been gaining attention due to their ability to improve growth performance and carcass quality, prevent gastrointestinal infection and most importantly, their ‘generally recognized as safe’ status. Previous studies support the potential of lactobacilli to regulate host immune systems, enhance gut metabolic capacities and maintain balance in the gut microbiota. Research on swine gut microbiota has revealed complex gut microbial community structure and showed the importance of Lactobacillus to the host's health. However, the species‐ and strain‐specific characteristics of lactobacilli that confer probiotic benefits are still not well understood. The diversity of probiotic traits in a complex gut ecosystem makes it challenging to infer the relationships between specific functions of Lactobacillus sp. and host health. In this review, we provide an overview of how lactobacilli play a pivotal role in the swine gut ecosystem and identify key characteristics that influence gut microbial community structure and the health of pigs. In addition, based on recent and ongoing meta‐omics and omics research on the gut microbiota of pigs, we suggest a workflow combining culture‐dependent and culture‐independent approaches for more effective selection of probiotic lactobacilli.     

An unusual symbiont from the gut of surgeonfishes may be the largest known prokaryote.

Symbionts first reported from the gut of a Red Sea surgeonfish, Acanthurus nigrofuscus (family Acanthuridae), were subsequently described as Epulopiscium fishelsoni. The taxonomic position of this very large (up to 576 microns in length) microorganism has previously been designated in the literature as either uncertain or eukaryotic. We suggest that similar symbionts from Great Barrier Reef surgeonfish may be prokaryotes, which together with E. fishelsoni from the Red Sea may represent the largest known forms of this cell type. Features identifying the symbionts as prokaryotes include the presence of bacterial-type flagella and a bacterial nucleoid and the absence of a nucleus or any other membrane-bound organelle.     

Population genomic response to geographic gradients by widespread and endemic fishes of the Arabian Peninsula

Genetic structure within marine species may be driven by local adaptation to their environment, or alternatively by historical processes, such as geographic isolation. The gulfs and seas bordering the Arabian Peninsula offer an ideal setting to examine connectivity patterns in coral reef fishes with respect to environmental gradients and vicariance. The Red Sea is characterized by a unique marine fauna, historical periods of desiccation and isolation, as well as environmental gradients in salinity, temperature, and primary productivity that vary both by latitude and by season. The adjacent Arabian Sea is characterized by a sharper environmental gradient, ranging from extensive coral cover and warm temperatures in the southwest, to sparse coral cover, cooler temperatures, and seasonal upwelling in the northeast. Reef fish, however, are not confined to these seas, with some Red Sea fishes extending varying distances into the northern Arabian Sea, while their pelagic larvae are presumably capable of much greater dispersal. These species must therefore cope with a diversity of conditions that invoke the possibility of steep clines in natural selection. Here, we test for genetic structure in two widespread reef fish species (a butterflyfish and surgeonfish) and eight range‐restricted butterflyfishes across the Red Sea and Arabian Sea using genome‐wide single nucleotide polymorphisms. We performed multiple matrix regression with randomization analyses on genetic distances for all species, as well as reconstructed scenarios for population subdivision in the species with signatures of isolation. We found that (a) widespread species displayed more genetic subdivision than regional endemics and (b) this genetic structure was not correlated with contemporary environmental parameters but instead may reflect historical events. We propose that the endemic species may be adapted to a diversity of local conditions, but the widespread species are instead subject to ecological filtering where different combinations of genotypes persist under divergent ecological regimes.     

Gut microbiota of invasive bullfrog tadpoles responds more rapidly to temperature than a noninvasive congener

Environmental temperature can alter the composition, diversity, and function of ectothermic vertebrate gut microbial communities, which may result in negative consequences for host physiology, or conversely, increase phenotypic plasticity and persistence in harsh conditions. The magnitude of either of these effects will depend on the length of time animals are exposed to extreme temperatures, and how quickly the composition and function of the gut microbiota can respond to temperature change. However, the temporal effects of temperature on gut microbiota are currently unknown. Here, we investigated the length of time required for increased temperature to alter the composition of gut bacterial communities in tadpoles of two frog species, the green frog, Lithobates clamitans, and its congener, the globally invasive American bullfrog, L. catesbeianus. We also explored the potential functional consequences of these changes by comparing predicted metagenomic profiles across temperature treatments at the last experimental time point. Bullfrog‐associated microbial communities were more plastic than those of the green frog. Specifically, bullfrog communities were altered by increased temperature within hours, while green frog communities took multiple days to exhibit significant changes. Further, over ten times more bullfrog bacterial functional pathways were temperature‐dependent compared to the green frog. These results support our hypothesis that bullfrog gut microbial communities would respond more rapidly to temperature change, potentially bolstering their ability to exploit novel environments. More broadly, we have revealed that even short‐term increases in environmental temperature, expected to occur frequently under global climate change, can alter the gut microbiota of ectothermic vertebrates.     

The determinants of species richness of a relatively young coral-reef ichthyofauna

Aim Unique topographic features left the Red Sea and its north‐eastern extension into the Gulf of Aqaba practically devoid of coral‐reef‐based organisms during the last glacial maximum. The current ichthyofauna in these two ‘regions’ thus represents the product of relatively recent colonization by species found in the Arabian Sea, which adjoins the Red Sea at its southern tip. We used this system to test why some marine species seemingly fail to extend their geographic range, thereby generating spatial heterogeneity in biodiversity. Location The Arabian Sea, Red Sea, and the Gulf of Aqaba. Methods A list of coral‐reef‐associated fish species, belonging to the 10 most speciose families, was compiled for each region using published sources. The data were analysed (major axis regression, randomization tests) for taxonomic and body‐size‐dependent biases in colonization probabilities. A simple probabilistic model was used to examine the potential contribution of local (within‐region) extinctions to determining species composition in the Red Sea. Results Of the 462 reef‐associated species that inhabit the Arabian Sea, 69% have crossed successfully into the Red Sea; of these, 55% have crossed into the Gulf of Aqaba. A species’ probability of being found in either ‘target’ was independent of presumed innate differences, i.e. ecological correlates of taxonomic affiliation and body size. Similarly, local extinctions were found unlikely to have been of consequence over the past several thousand years. Main conclusions Present‐day differences in the species richness of reef‐associated fish species among the Arabian Sea, Red Sea and Gulf of Aqaba appear to be the product of external, non‐selective constraints on colonization. The random nature of the colonization process is suggestive of ecological redundancy among coral‐reef fish species. Importantly, the study places a time frame on the processes that determine spatial patterns of biodiversity in reef fish.     

Major Histocompatibility Complex class IIb polymorphism influences gut microbiota composition and diversity

Animals harbour diverse communities of symbiotic bacteria, which differ dramatically among host individuals. This heterogeneity poses an immunological challenge: distinguishing between mutualistic and pathogenic members of diverse and host‐specific microbial communities. We propose that Major Histocompatibility class II (MHC) genotypes contribute to recognition and regulation of gut microbes, and thus, MHC polymorphism contributes to microbial variation among hosts. Here, we show that MHC IIb polymorphism is associated with among‐individual variation in gut microbiota within a single wild vertebrate population of a small fish, the threespine stickleback. We sampled stickleback from Cedar Lake, on Vancouver Island, and used next‐generation sequencing to genotype the sticklebacks’ gut microbiota (16S sequencing) and their MHC class IIb exon 2 sequences. The presence of certain MHC motifs was associated with altered relative abundance (increase or decrease) of some microbial Families. The effect sizes are modest and entail a minority of microbial taxa, but these results represent the first indication that MHC genotype may affect gut microbiota composition in natural populations (MHC‐microbe associations have also been found in a few studies of lab mice). Surprisingly, these MHC effects were frequently sex‐dependent. Finally, hosts with more diverse MHC motifs had less diverse gut microbiota. One implication is that MHC might influence the efficacy of therapeutic strategies to treat dysbiosis‐associated disease, including the outcome of microbial transplants between healthy and diseased patients. We also speculate that macroparasite‐driven selection on MHC has the potential to indirectly alter the host gut microbiota, and vice versa.     

Intestinal microbiota in fishes: what's known and what's not

High‐throughput sequencing approaches have enabled characterizations of the community composition of numerous gut microbial communities, which in turn has enhanced interest in their diversity and functional relationships in different groups of vertebrates. Although fishes represent the greatest taxonomic and ecological diversity of vertebrates, our understanding of their gut microbiota and its functional significance has lagged well behind that of terrestrial vertebrates. In order to highlight emerging issues, we provide an overview of research on fish gut microbiotas and the biology of their hosts. We conclude that microbial community composition must be viewed within an informed context of host ecology and physiology, and that this is of particular importance with respect to research planning and sampling design.     

Individuals' diet diversity influences gut microbial diversity in two freshwater fish (threespine stickleback and Eurasian perch)

Vertebrates' diets profoundly influence the composition of symbiotic gut microbial communities. Studies documenting diet‐microbiota associations typically focus on univariate or categorical diet variables. However, in nature individuals often consume diverse combinations of foods. If diet components act independently, each providing distinct microbial colonists or nutrients, we expect a positive relationship between diet diversity and microbial diversity. We tested this prediction within each of two fish species (stickleback and perch), in which individuals vary in their propensity to eat littoral or pelagic invertebrates or mixtures of both prey. Unexpectedly, in most cases individuals with more generalised diets had less diverse microbiota than dietary specialists, in both natural and laboratory populations. This negative association between diet diversity and microbial diversity was small but significant, and most apparent after accounting for complex interactions between sex, size and diet. Our results suggest that multiple diet components can interact non‐additively to influence gut microbial diversity.     

Sources of variation in community composition of the hindgut microbiota in two tropical Kyphosus species

Gut microbiota play a fundamental role in the nutrition of many vertebrate herbivores through foregut and hindgut fermentation of plant carbohydrates. Some species of marine herbivorous fishes contain moderate to high levels of short-chain fatty acids in the hindgut, indicating the importance of hindgut fermentation. Herbivorous fish hindgut microbiota are diverse and can vary with geographic location, but data on the scale of geographic variation involving a few km of separation are limited. Here, we used the 16S rRNA gene to describe community composition of the gut microbiota of the herbivorous species Kyphosus vaigiensis and K. cinerascens collected in the vicinity of Lizard Island, northern Great Barrier Reef, Australia, in 2011 and 2017. Microbiota community structure differed between posterior hindgut sections, host species, sampling years and two mid-shelf and outer reef locations approximately 20 km apart. Hindgut bacterial community composition varied remarkably between mid-shelf and outer reef locations, and among individual fish on the mid-shelf reef. In both fish species, the most abundant phyla were Pseudomonadota, Bacillota and Bacteroidota, followed by Spirochaetota, Thermodesulfobacteriota and Verrucomicrobiota. There were no clear differences between the host species in terms of the relative abundance and composition of bacterial genera in outer reef samples. In contrast, the dominant genera differed between mid-shelf samples of K. cinerascens and K. vaigiensis, being Endozoicomonas-like (Pseudomonadota) and Brevinema (Spirochaetota), respectively. Endozoicomonas are emerging as important symbionts in many marine hosts worldwide and are thought to be important in the coral sulphur cycle. Differences in microbiota composition were not associated with variation in fish condition, suggesting that the different microbial taxa perform equivalent functional roles.

     

The Reproductive Behavior of Acanthurus nigrofuscus (Forskal) and other Surgeonfishes (Fam. Acanthuridae) off Eilat,Israel (Gulf of Aqaba,Red Sea)

The reproductive behavior of Acanthurus nigrofuscus, a common surgeonfish of the Red Sea, is described for two overlapping populations inhabiting the coral reefs off Eilat, Israel (Gulf of Aqaba). The spectacular daily spawning activities, often involving aggregations of thousands of individuals, as well as the often long distance migrations to and from the spawning grounds by groups in highly organized formations are characterized in detail. Evidence is provided that the precise timing of these various phenomena is controlled by ambient light levels during the late afternoon. Less detailed information is also provided on comparable activities of two other surgeonfishes from the same reefs: Ctenochaetus striatus and Zebrasoma xanthurum. Finally, comparisons are made of reproduction and its associated environmental controls among populations of the same and related species of surgeonfishes at widely distributed locations in the Indo-Pacific.     

Recruitment of coral reef fishes along a cross-shelf gradient in the Red Sea peaks outside the hottest season

Knowledge on the early life history, ecology, and biology of marine species is crucial for future projections of the resilience of coral reef ecosystems and for adequate management strategies. A fundamental component of population dynamics is the recruitment of new individuals, and in some marine populations, this may be a limiting factor. Recruitment peaks of coral reef fishes commonly occur during the warmer months of the year in many subtropical and temperate locations worldwide. In the Red Sea, very little is known about the influence of temperature on reproductive patterns of coral reef fishes and studies on recruitment are missing. The Red Sea is one of the hottest and most isolated tropical seas in the world. We hypothesized that sea surface temperatures (SSTs) during the Red Sea’s hottest season may exceed the optimum for successful recruitment of some coral reef fishes, which therefore has to occur during other, cooler seasons, unlike recruitment among coral reef ecosystems around the world. We identified taxa among fish recruits by matching mitochondrial DNA sequences (using COI, commonly known as “barcoding”) and assessed potential biological and environmental drivers of recruitment. We studied three reefs located along a cross-shelf gradient for 12 consecutive months in the central Red Sea to capture seasonal changes in biotic and abiotic parameters along this gradient. Our results indicated that recruitment peaks did not occur during the hottest SSTs for most taxa, especially at the hottest inshore and mid-shelf reefs, and identified fish recruitment to be mainly and strongly correlated with the biomass of planktonic invertebrates. Moreover, temporal patterns of fish recruitment differed within and among taxonomic families among the reefs.

     

The fish assemblage on a coralligenous shallow shelf off the Mediterranean coast of northern Israel

The fish assemblage on the shallow coralligenous shelf (16-30m depth) off Haifa, Israel was sampled using trammel nets throughout a period of 1 year. Complementary data were obtained via underwater censuses of fish on an artificial reef established later in the sampling area. Fortythree species of fish were sampled by trammel nets, 79% of which were observed also during the underwater censuses. Although fish of Red Sea origin constituted only 11.6% of the species composition in the net samples, they contributed 46.2% of the fish abundance and 40.6% of the biomass in these samples. This was supported by the finding that species of Red Sea origin contributed 64% of the abundance of large fish counted on the artificial reef. Siganus luridas, S. rivulatus and Sargocentron rubrum are the main contributors in number and biomass among fish of Red Sea origin. It is suggested that the biogenic rocky bottom of this area contains several components which are similar to biogenic habitats favoured by these benthic species in the Red Sea; this may explain the high abundance of these species in the studied area.     

Gut microbial diversity across a contact zone for California voles: Implications for lineage divergence of hosts and mitonuclear mismatch in the assembly of the mammalian gut microbiome

Gut microbial diversity is thought to reflect the co‐evolution of microbes and their hosts as well as current host‐specific attributes such as genetic background and environmental setting. To explore interactions among these parameters, we characterized variation in gut microbiome composition of California voles (Microtus californicus) across a contact zone between two recently diverged lineages of this species. Because this contact zone contains individuals with mismatched mitochondrial‐nuclear genomes (cybrids), it provides an important opportunity to explore how different components of the genotype contribute to gut microbial diversity. Analyses of bacterial 16S rRNA sequences and joint species distribution modelling revealed that host genotypes and genetic differentiation among host populations together explained more than 50% of microbial community variation across our sampling transect. The ranked importance (most to least) of factors contributing to gut microbial diversity in our study populations were: genome‐wide population differentiation, local environmental conditions, and host genotypes. However, differences in microbial communities among vole populations (β‐diversity) did not follow patterns of lineage divergence (i.e., phylosymbiosis). Instead, among‐population variation was best explained by the spatial distribution of hosts, as expected if the environment is a primary source of gut microbial diversity (i.e., dispersal limitation hypothesis). Across the contact zone, several bacterial taxa differed in relative abundance between the two parental lineages as well as among individuals with mismatched mitochondrial and nuclear genomes. Thus, genetic divergence among host lineages and mitonuclear genomic mismatches may also contribute to microbial diversity by altering interactions between host genomes and gut microbiota (i.e., hologenome speciation hypothesis).     

The inconstant gut microbiota of Drosophila species revealed by 16S rRNA gene analysis

The gut microorganisms in some animals are reported to include a core microbiota of consistently associated bacteria that is ecologically distinctive and may have coevolved with the host. The core microbiota is promoted by positive interactions among bacteria, favoring shared persistence; its retention over evolutionary timescales is evident as congruence between host phylogeny and bacterial community composition. This study applied multiple analyses to investigate variation in the composition of gut microbiota in drosophilid flies. First, the prevalence of five previously described gut bacteria (Acetobacter and Lactobacillus species) in individual flies of 21 strains (10 Drosophila species) were determined. Most bacteria were not present in all individuals of most strains, and bacterial species pairs co-occurred in individual flies less frequently than predicted by chance, contrary to expectations of a core microbiota. A complementary pyrosequencing analysis of 16S rRNA gene amplicons from the gut microbiota of 11 Drosophila species identified 209 bacterial operational taxonomic units (OTUs), with near-saturating sampling of sequences, but none of the OTUs was common to all host species. Furthermore, in both of two independent sets of Drosophila species, the gut bacterial community composition was not congruent with host phylogeny. The final analysis identified no common OTUs across three wild and four laboratory samples of D. melanogaster. Our results yielded no consistent evidence for a core microbiota in Drosophila. We conclude that the taxonomic composition of gut microbiota varies widely within and among Drosophila populations and species. This is reminiscent of the patterns of bacterial composition in guts of some other animals, including humans.     

Diet drives convergent evolution of gut microbiomes in bamboo-eating species

Gut microbiota plays a critical role in host physiology and health. The coevolution between the host and its gut microbes facilitates animal adaptation to its specific ecological niche. Multiple factors such as host diet and phylogeny modulate the structure and function of gut microbiota. However, the relative contribution of each factor in shaping the structure of gut microbiota remains unclear. The giant(Ailuropoda melanoleuca) and red(Ailurus styani) pandas belong to different families of order Carnivora. They have evolved as obligate bamboo-feeders and can be used as a model system for studying the gut microbiome convergent evolution. Here, we compare the structure and function of gut microbiota of the two pandas with their carnivorous relatives using 16S rRNA and metagenome sequencing. We found that both panda species share more similarities in their gut microbiota structure with each other than each species shares with its carnivorous relatives. This indicates that the specialized herbivorous diet rather than host phylogeny is the dominant driver of gut microbiome convergence within Arctoidea.Metagenomic analysis revealed that the symbiotic gut microbiota of both pandas possesses a high level of starch and sucrose metabolism and vitamin B12 biosynthesis. These findings suggest a diet-driven convergence of gut microbiomes and provide new insight into host-microbiota coevolution of these endangered species.     

Kenyan coral reef lagoon fish: effects of fishing,substrate complexity,and sea urchins

Population density, number of species, diversity, and species-area relationships of fish species in eight common coral reef-associated families were studied in three marine parks receiving total protection from fishing, four sites with unregulated fishing, and one reef which recently received protection from fishing (referred to as a transition reef). Data on coral cover, reef topographic complexity, and sea urchin abundance were collected and correlated with fish abundance and species richness. The most striking result of this survey is a consistent and large reduction in the population density and species richness of 5 families (surgeonfish, triggerfish, butterflyfish, angelfish, and parrotfish). Poor recovery of parrotfish in the transition reef, relative to other fish families, is interpreted as evidence for competitive exclusion of parrotfish by sea urchins. Reef substrate complexity is significantly associated with fish abundance and diversity, but data suggest different responses for protected versus fished reefs, protected reefs having higher species richness and numbers of individuals than unprotected reefs for the same reef complexity. Sea urchin abundance is negatively associated with numbers of fish and fish species but the interrelationship between sea urchins, substrate complexity, coral cover, and management make it difficult to attribute a set percent of variance to each factor-although fishing versus no fishing appears to be the strongest variable in predicting numbers of individuals and species of fish, and their community similarity. Localized species extirpation is evident for many species on fished reefs (for the sampled area of 1.0 ha). Fifty-two of 110 species found on protected reefs were not found on unprotected reefs.     

饮食因素对肠道菌群影响的研究进展

人体肠道内定植了约1014个微生物,种类有1 000多种,它们作为"人体的第十三个生理系统",直接参与了机体的各种代谢活动,与人体健康密切相关。研究显示,肠道菌群的构成和稳定受到诸多宿主和环境因素的影响,其中饮食因素起着至关重要的作用。因此,本文用膳食金字塔将食物进行分类,介绍了膳食中谷类、果蔬类、豆类、奶类、鱼肉类、油脂类和糖类对肠道菌群的调节作用,以期为相关研究的开展、相应疾病的防治提供参考。