Papers by Mary Beth Saffo
Integrative and Comparative Biology, Apr 1, 2002
SYNOPSIS. Research on symbiosis (including antagonistic and mutualistic associations) wrestles, d... more SYNOPSIS. Research on symbiosis (including antagonistic and mutualistic associations) wrestles, directly or indirectly, with the paradox: why are symbiotic associations so prevalent in the biosphere in the face of ubiquitous immune or antibiotic defenses among organisms? The symposium ''Living Together: the Dynamics of Symbiotic Interactions'' considered several questions: 1. How do symbiotic species partners come together? Do symbioses share similar patterns of signal recognition and response? 2. What roles do nutrients and metabolites play in symbiotic interactions, and how are metabolic exchanges affected by environmental changes? 3. In what ways do the dynamics of multispecies symbioses differ from two-species associations? 4. How do antagonistic (parasitic, pathogenic) symbioses differ from mutualistic ones? In what ways do changes in the biotic and physical environment affect the evolutionary balance of symbiotic associations? 5. What are the coevolutionary patterns of symbiotic associations? 6. Which research techniques, and strategies of experimental design, might be useful across a broad range of symbiotic associations? Two themes emerged from the symposium. First, all the participants have incorporated multiple techniques and perspectives into their work, approaches which facilitate the understanding of symbiotic dynamics at several levels of biological organization. Secondly, many of the papers addressed genetic and environmental variation in symbiotic interactions. Such approaches are useful tools for analysis of the mechanics of interspecies interactions and for characterization of the most important factors which influence them. They provide us with the tools to evaluate symbioses in a world of complexity, variation and change. Nothing unconnected ever occurs.-sign on a church, Cambridge, Massachusetts So essential is the property of self/non-self recognition to life, and so ingrained is the perspective that absence of infection is a requisite of organismal health, that symbiotic interactions (protracted, intimate associations between two or more species: Saffo, 1992b) continue to surprise us, even as we continue to document the ubiquitous distribution of symbioses in the biosphere. We are intrigued by these apparent exceptions to our axenic rule, by ways in which species can live for extended periods in close association with another-often inside another-despite immune defenses which should make such ways of life improbable or impossible. Perhaps in part because of the diversity of these ''exceptions,'' as well as the technical complexities of studying symbiotic interactions, researchers have tended to focus empirical work on individual symbioses, and on their implications for the particular taxa involved, or the ecological, evolutionary, nutritional, medical or agricultural relevance of each. There is no doubt that each symbiosis provides particular points of fascination, and each offers particular developmental, physiological, evolutionary or ecological lessons for us. Consider these few examples.
Laboratory mammals have served as key experimental models for a number of human diseases, but the... more Laboratory mammals have served as key experimental models for a number of human diseases, but they have been less useful in the study of urolithiasis. Because they do not produce uric acid as an end product of purine catabolism, most mammals are especially limited models for uric acid urolithiasis and of mixed urate-oxalate stones.
Marine Biology, Jun 1, 1990
The marine protistNephromyces Giard, 1888 is a chronic endosymbiont of molgulid tunicates. Ultras... more The marine protistNephromyces Giard, 1888 is a chronic endosymbiont of molgulid tunicates. Ultrastructural and cytochemical studies of this protist, isolated from molgulid hosts collected from the Pacific, Atlantic and Gulf Coasts of the United States, indicate thatNephromyces is itself chronically infected with Gramnegative, intracellular bacteria. Molgulid tunicates are thus the locus of a nested,tripartite endosymbiosis. Intracellular bacteria are present in both trophic and reproductive stages ofNephromyces, suggesting that the bacterial-Nephromyces symbiosis is an hereditary association. The presence of endosymbionts inNephromyces raises the possibility that some ofNephromyces' metabolic characteristics, in particular its high urate oxidase activity, might be supplied not byNephromyces itself, but rather by its intracellular bacteria, possibly functioning as peroxisomal analogues.
eLS, Jul 15, 2014
The authors review the theoretical and experimental evidence supporting exploitation as an altern... more The authors review the theoretical and experimental evidence supporting exploitation as an alternative route to the evolution of mutualistic symbioses.
Canadian journal of botany, Jul 1, 1986
The endosymbiotic marine protist Nephromyces was first classified as a chytridiomycete by Giard i... more The endosymbiotic marine protist Nephromyces was first classified as a chytridiomycete by Giard in 1888, yet its taxonomic affinities with chytridiomycetes, as well as with other groups traditionally considered fungi, remain in doubt. To supplement the morphological data on which taxonomic inferences have been based, we assayed Nephromyces for chitin, using three methods: chromatographic assays of acid hydrolysates of alkali-resistant cell residues; infrared spectral analysis; and observations of N-acetylglucosamine-specific lectin-binding properties of the surfaces of living cells. All three assays indicate the presence of chitin in Nephromyces. The possible phylogenetic implications of this finding are discussed.
The Biological Bulletin, Feb 1, 1982
The renal sac of the sea squirt Molgula manhattensis consistently harbors a collection of fungus-... more The renal sac of the sea squirt Molgula manhattensis consistently harbors a collection of fungus-like cells, "'Nephromyces'". These cells are not Molgula cells, but an organism(s) foreign to the host. Nephromyces does not have an obligate intermediate host. Nephromyces is not transmitted with the gametes of Molgula, but can be transmitted to Molgula through the ambient water. Nephromyces is released into the water after death of its host, although not necessarily only at this time. Molgula acquires Nephromyces after the initiation of feeding, which follows settling and metamorphosis. Nephromyces remains infective for at least twentynine days after isolation from its host.
Journal of Morphology, Mar 1, 1978
The renal sac of the ascidian family Molgulidae (Tunicata, phylum Chordata) has been thought to f... more The renal sac of the ascidian family Molgulidae (Tunicata, phylum Chordata) has been thought to function as a kidney, yet its structure, contents and activities seem incompatible with current generalizations regarding excretory processes in marine animals. The development of the renal sac is described here as part of a general effort to reexamine the organ's role in Molgula manhattensis. Light microscopy of living animals and fixed material has shown the following: (1) The renal sac begins to sequester concretions before the heart starts beating and before feeding begins. Therefore, blood circulation by heartbeat is not necessary for production or transport of the initial concretions, whatever its effects may be on the renal sac in older individuals. Ingested food cannot provide the initial concretion material. (2) In laboratory‐raised animals, concretions appear in the renal sac before “renal sac organisms” (fungus‐like organisms seen in the renal sac of all field‐collected adults) can be detected. Thus, at least some portion of the concretions can be produced by Molgula in the absence of renal sac organisms. (3) No openings have been detected in the renal sac at any stage of its development, nor is there any evidence that concretions are dissolved or transported out of the renal sac. (4) The development and morphology of the renal sac are consistent with the hypothesis that the organ is an epicardial derivative, except that the renal sac arises from post‐pharyngeal (presumptive gut) endoderm, rather than pharyngeal endoderm.
Science, Jun 9, 1978
Weddellite (calcium oxalate dihydrate) and calcite (anhydrous calcium carbonate phase) are compon... more Weddellite (calcium oxalate dihydrate) and calcite (anhydrous calcium carbonate phase) are components of concretions in the renal sac of the ascidian tunicate Molgula manhattensis. The presence of weddellite along with urate in the concretions suggests a resemblance to human kidney stones, although, unlike the latter, the concretions in Molgula do not seem to be pathologic deposits.
Genome Biology and Evolution, Jul 22, 2019
Data deposition: Sequencing data were deposited in NCBI GenBank under the BioProject PRJNA524113.... more Data deposition: Sequencing data were deposited in NCBI GenBank under the BioProject PRJNA524113. The Nephromyces-enriched renal sac metagenome and metatranscriptome of Molgula occidentalis were deposited in NCBI GenBank under the accessions SOZB00000000.1 and GHIL00000000.1. Raw sequencing reads were deposited on the NCBI SRA archive under the accessions SRR8618777, SRR8618778, SRR8618779, and SRR8618780. Multi-gene data sets as well as phylogenetic trees inferred in this study were deposited at Mendeley Data under the
BioSystems, 1981
This paper reviews current knowledge concerning the identity of Nephromycez, a collection of fung... more This paper reviews current knowledge concerning the identity of Nephromycez, a collection of fungus-like cells found in the renal sac of all molgulid tunicates thus far examined. The following has been demonstrated: (1) The cells called Nephromyces do exist, and are not produced by their tunicate hosts, but are something foreign to these animals. (2) Many forms of "Nephromyces" cells are present simultaneously in the renal sac of adults of each molguUd species. Despite their extraordinarily eclectic appearance, all these cells are part of the same life cycle. (3) Initial ultrastructural data indicate that Nephromyces is a eukaryote. They also suggest that, despite the speculations of early authors, Nephromyces may not be a Chytridiomycete.
Genome Biology and Evolution, Nov 30, 2018
The phylum Apicomplexa is a quintessentially parasitic lineage, whose members infect a broad rang... more The phylum Apicomplexa is a quintessentially parasitic lineage, whose members infect a broad range of animals. One exception to this may be the apicomplexan genus Nephromyces, which has been described as having a mutualistic relationship with its host. Here we analyze transcriptome data from Nephromyces and its parasitic sister taxon, Cardiosporidium, revealing an ancestral purine degradation pathway thought to have been lost early in apicomplexan evolution. The predicted localization of many of the purine degradation enzymes to peroxisomes, and the in silico identification of a full set of peroxisome proteins, indicates that loss of both features in other apicomplexans occurred multiple times. The degradation of purines is thought to play a key role in the unusual relationship between Nephromyces and its host. Transcriptome data confirm previous biochemical results of a functional pathway for the utilization of uric acid as a primary nitrogen source for this unusual apicomplexan.
BioScience, Apr 1, 1996
bilities nor impacts of environmental changes at the ecosystem level can be evaluated. The writin... more bilities nor impacts of environmental changes at the ecosystem level can be evaluated. The writing is comprehensive and up to date because of the combined efforts of 28 leading researchers of plant ecophysiology-no cha pter was written by a single author. The book is likely to be welcomed by investigators attempting to unravel the complexities inherent in biological diversity, global warming, and responses of forest ecosystems to a biotic and biotic stresses.
American zoologist, Aug 1, 1992
SYNOPSIS. Endosymbiosis is a phenomenon of central importance to the biology of many invertebrate... more SYNOPSIS. Endosymbiosis is a phenomenon of central importance to the biology of many invertebrate animals. Parasitic, commensal and mutualistic endosymbioses are widely distributed among invertebrate taxa, and have arguably played a major role in the evolution of several invertebrate families, classes and phyla. Sometimes accounting for as much as 50% of invertebrate volume or biomass, endosymbionts can profoundly affect the ecology, physiology, development and behavior of invertebrate hosts. Endosymbiosis raises a number of questions that are worth the serious, sustained attention of a broad range of invertebrate biologists.
The Phylum Apicomplexa is a quintessentially parasitic lineage, whose members infect a broad rang... more The Phylum Apicomplexa is a quintessentially parasitic lineage, whose members infect a broad range of animals. One exception to this may be the apicomplexan genus Nephromyces, which has been described as having a mutualistic relationship with its host. Here we analyze transcriptome data from Nephromyces and its parasitic sister taxon, Cardiosporidium, revealing an ancestral purine degradation pathway thought to have been lost early in apicomplexan evolution. The predicted localization of many of the purine degradation enzymes to peroxisomes, and the in silico identification of a full set of peroxisome proteins, indicates that loss of both features in other apicomplexans occurred multiple times. The degradation of purines is thought to play a key role in the unusual relationship between Nephromyces and its host. Transcriptome data confirm previous biochemical results of a functional pathway for the utilization of uric acid as a primary nitrogen source for this unusual apicomplexan
Proceedings of the National Academy of Sciences, 2010
With malaria parasites ( Plasmodium spp.), Toxoplasma , and many other species of medical and vet... more With malaria parasites ( Plasmodium spp.), Toxoplasma , and many other species of medical and veterinary importance its iconic representatives, the protistan phylum Apicomplexa has long been defined as a group composed entirely of parasites and pathogens. We present here a report of a beneficial apicomplexan: the mutualistic marine endosymbiont Nephromyces . For more than a century, the peculiar structural and developmental features of Nephromyces , and its unusual habitat, have thwarted characterization of the phylogenetic affinities of this eukaryotic microbe. Using short-subunit ribosomal DNA (SSU rDNA) sequences as key evidence, with sequence identity confirmed by fluorescence in situ hybridization (FISH), we show that Nephromyces , originally classified as a chytrid fungus, is actually an apicomplexan. Inferences from rDNA data are further supported by the several apicomplexan-like structural features in Nephromyces , including especially the strong resemblance of Nephromyces i...
SYNOPSIS. Research on symbiosis (including antagonistic and mutualistic associations) wrestles, d... more SYNOPSIS. Research on symbiosis (including antagonistic and mutualistic associations) wrestles, directly or indirectly, with the paradox: why are symbiotic associations so prevalent in the biosphere in the face of ubiquitous immune or antibiotic defenses among organisms? The symposium ''Living Together: the Dynamics of Symbiotic Interactions'' considered several questions: 1. How do symbiotic species partners come together? Do symbioses share similar patterns of signal recognition and response? 2. What roles do nutrients and metabolites play in symbiotic interactions, and how are metabolic exchanges affected by environmental changes? 3. In what ways do the dynamics of multispecies symbioses differ from two-species associations? 4. How do antagonistic (parasitic, pathogenic) symbioses differ from mutualistic ones? In what ways do changes in the biotic and physical environment affect the evolutionary balance of symbiotic associations? 5. What are the coevolutionary patterns of symbiotic associations? 6. Which research techniques, and strategies of experimental design, might be useful across a broad range of symbiotic associations? Two themes emerged from the symposium. First, all the participants have incorporated multiple techniques and perspectives into their work, approaches which facilitate the understanding of symbiotic dynamics at several levels of biological organization. Secondly, many of the papers addressed genetic and environmental variation in symbiotic interactions. Such approaches are useful tools for analysis of the mechanics of interspecies interactions and for characterization of the most important factors which influence them. They provide us with the tools to evaluate symbioses in a world of complexity, variation and change. Nothing unconnected ever occurs.-sign on a church, Cambridge, Massachusetts So essential is the property of self/non-self recognition to life, and so ingrained is the perspective that absence of infection is a requisite of organismal health, that symbiotic interactions (protracted, intimate associations between two or more species: Saffo, 1992b) continue to surprise us, even as we continue to document the ubiquitous distribution of symbioses in the biosphere. We are intrigued by these apparent exceptions to our axenic rule, by ways in which species can live for extended periods in close association with another-often inside another-despite immune defenses which should make such ways of life improbable or impossible. Perhaps in part because of the diversity of these ''exceptions,'' as well as the technical complexities of studying symbiotic interactions, researchers have tended to focus empirical work on individual symbioses, and on their implications for the particular taxa involved, or the ecological, evolutionary, nutritional, medical or agricultural relevance of each. There is no doubt that each symbiosis provides particular points of fascination, and each offers particular developmental, physiological, evolutionary or ecological lessons for us. Consider these few examples.
SYNOPSIS. Research on symbiosis (including antagonistic and mutualistic associations) wrestles, d... more SYNOPSIS. Research on symbiosis (including antagonistic and mutualistic associations) wrestles, directly or indirectly, with the paradox: why are symbiotic associations so prevalent in the biosphere in the face of ubiquitous immune or antibiotic defenses among organisms? The symposium ‘‘Living Together: the Dynam-ics of Symbiotic Interactions’ ’ considered several questions: 1. How do symbiotic species partners come together? Do symbioses share similar patterns of signal recognition and response? 2. What roles do nutrients and metabolites play in symbiotic interactions, and how are metabolic exchanges affected by environmental changes? 3. In what ways do the dynamics of multispecies symbioses differ from two-species associations? 4. How do antagonistic (parasitic, pathogenic) symbioses differ from mutualistic ones? In what ways do changes in the biotic and physical environment affect the evolutionary balance of symbiotic associations? 5. What are the coevolutionary patterns of symbi...
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Papers by Mary Beth Saffo