Moselio Schaechter

  • The purpose of this blog is to share my appreciation for the width and depth of the microbial activities on this planet. I will emphasize the unusual and the unexpected phenomena for which I have a special fascination... (more)

    For the memoirs of my first 21 years of life, click here.

Associate Bloggers

  • (Click photo for more information.)

Bloggers Emeriti

  • (Click photo for more information.)

Meetings & Sponsors

April 22, 2014

The Tale of a Tubeworm and a Biofilm

by Jordan Kesner, Bryan Hancock, and Nicole Nalbandian

Figure1 Figure 1. Tubeworm Life Stages. Left, larva of H. elegans. Right, Adult H. elegans with tube. Courtesy of Brian Nedved.

The oceans of our world harbor an incredible diversity of life, the vast majority of which has yet to be observed or characterized. This is part of what makes the study of marine biology so exciting; there is, in essence, an endless sea of new and exciting underwater discoveries to be made. When a biologist thinks of the creatures that inhabit our oceans, one of the prominent examples that often comes to mind is the tubeworm, a metazoan with a characteristic tube-like outer shell. The most likely image one thinks of is of the giant chemosynthetic tubeworms inhabiting the darkest recesses of the oceans near hydrothermal vents. In fact, many different species of tubeworms exist in the various regions of the ocean, and they are often involved in complex symbiotic relationships with other forms of marine life. The elongated, calcified, tube-like ‘shell’ in which adult worms live actually only represents half of their life cycle. They also exist in the juvenile state as free-swimming larvae, which actively seek out new surfaces to colonize. When a tubeworm larva decides it has found a good spot to settle, it initiates metamorphosis that results in anchoring itself to a solid substrate and begin growing into an adult worm.  After the adult worms release gametes into the water, they join to form new larvae, thus completing the life cycle.

Figure2 Figure 2. Colonies of P. luteo on agar. Courtesy of Nicholas Shikuma.

Bacterial Prodding

Recently, biologists have discovered that bacterial biofilms  are important participants in the life cycle of many marine invertebrates. For invertebrates such as the tubeworm, Hydroides elegans (well known by seafaring types for its role in biofouling), bacterial biofilms are known to produce a signal required by the larval stage of the worm to become able to settle and develop into a mature, stationary adult. When they receive this signal, the larvae of H. elegans embed themselves into the bacterial biofilm. H. elegans typicallylives in shallow waters in the so-called ‘benthic zone’, or lowest depth, where it shares an interesting relationship with a bacterium, Pseudoalteromonas luteoviolacea (P. luteo). Thisis a biofilm-forming bacterium that is responsible for inducing metamorphosis in H. elegans. Until recently, what this signal was and how it functioned remained enigmatic.

Figure3 Figure 3. Structural components of assembled MACs. Courtesy of Nicholas Shikuma.

Here we examine a recently published paper by Shikuma et al. that sheds light on this fascinating bacterium-tubeworm relationship. The authors took a close look at a cluster of genes found in P. luteo that had previously been identified as essential to their ability to induce metamorphosis in the tubeworm.  They found that some of the sequences resembled a family of bacterial genes encoding the bioactive agents called bacteriocins. Surprisingly, some bacteriocins share morphological and sequence similarity with the tail structures of phages. Many phage use contractile tails to breach the cellular envelopes of their bacterial hosts and gain access to the cytoplasm. The phage tail-like bacteriocins have all the tail components of a functional phage but without the DNA filled head of the virus, a most striking example of evolution leading to multiple uses of a biological structure.  And these structures are also used for a kind of bacterial protein secretion called Type VI or in the virulence of the bacterium Photorhabdus against moths. But, remarkably, phage tail-like structures have yet other uses. This paper shows convincingly that it is these structures that provide the signal for a beneficial activity, the initiation of metamorphosis in H. elegans. The authors appropriately name these proteins MACs, for Metamorphosis-Associated Contractile Structures.

Figure4 Figure 4. Mutant MACs do not induce metamorphosis. Source.

Surprises From Phage-like Tails

One of the most interesting aspects of this study was the elucidation of the physical structure of the MAC proteins. The MACs of P. luteo are made of four major proteins: the baseplate, the sheath, and two tube proteins, each encoded by a separate ORF.  In vitro, MACs are released extracellularly when a small percentage (approximately 2.4%) of the P. luteo in a biofilm population lyse. To investigate which components of the MAC complex are required for induction of metamorphosis, these researchers made mutants deficient in the MAC structural genes. Each construct contained a baseplate-GFP fusion protein to allow visualization of the released MACs. Next, they purified the MACs and added them to H. elegans. None of the mutant proteins were able to induce metamorphosis.This suggests that the full and intact MAC complex is required in the H. elegans lifecycle.

Figure5 Figure 5. Cryo-EM images of MAC Superstructure. Source.

Using cryoelectron microscopy, the group obtained stunning images of MACs in what is assumed to be a close representation of their native state. MACs do not function individually. Rather, they make highly ordered arrays that are held in place in supramolecular hexagonal lattices. This is the first time such a complex structure consisting of phage-like tails has ever been observed, and it may give insight into the native structures of related bacteriocins. The MAC tube protein appears to exist in one of two conformations thought to represent two different functional states: one in which the tube protein is still present in the MAC complex, and one in which it is missing. Based on this and knowledge of how phages inject their DNA into host cells, one could speculate that the MACs function as a molecular gun, irreversibly firing the tube protein into the cell membrane of the larva of H. elegans.  The nature of the stimulus that causes the MAC tube protein to be fired from the complex is not yet known. The novelty of the data produced by Shikuma et al. opens the door to many other exciting questions that the authors hope to answer in future studies. Some of these already come to mind: how exactly do MACs interact with the larvae, how is the tube fired from the complex, how many MACs are required to induce metamorphosis, what is the nature of the symbiosis between bacteria and tubeworm, how is the synthesis of the MACs regulated in the bacteria, and so forth.

Figure6 Figure 6. The two states of the molecular gun, MAC Complex. Source.

Novel Structures, Novel Signals

Preliminary data suggest that the hexagonal lattice protein that holds the MAC superstructure in place (termed MAC-L) is required for larval metamorphosis. This would seem to indicate that the large, multi-MAC complexes provide the signal, and that individual MAC complexes are not sufficient. The next step in this research will be to annotate the bacterial genome by knocking out specific segments of the genes associated with the MAC proteins. Doing so will allow identification of the key structural components required for the function of MACs. In his own words, Dr. Shikuma “would like to explore the direct interactions of P. luteo with H. elegans to determine precisely how the MAC complex interacts with the larvae.” He is also interested in exploring the phylogenetic diversity of various bacterial species that synthesize MACs.

The pioneering work done here paves the way for more intensive study into MACs and specifically of their relationship to animal life cycles. Who knows, such a structural bacterial element might carry out a beneficial function in humans. Wouldn't that be a novel and exciting concept? It does not seem too farfetched to think that MACs and phage tail-like structures may be useful to humans in the future. Maybe in agriculture, where MACs, in aiding certain organisms to complete their life cycle, may lead to propagation of new animal species in captivity and to other beneficial uses. Could MACs created in gut microbes mediate an immune response in the body? The future seems bright in MACland.



The authors of this paper are participants in the 2014 Winter quarter UCSD/SDSU Integrative Microbiology graduate course. The authors contributed equally to this work.

Note from the authors: This project would not have been possible without the collaborative effort of many people with a wide range of expertise; Special thanks to Michael Hadfield for his expertise in tubeworm biology and Martin Pilhofer for his electron microscopy work.

We sincerely thank Dr. Shikuma for meeting with us personally to answer all questions regarding the study.

Tran, C., & Hadfield, M. (2011). Larvae of Pocillopora damicornis (Anthozoa) settle and metamorphose in response to surface-biofilm bacteria Marine Ecology Progress Series, 433, 85-96 DOI: 10.3354/meps09192

Shikuma NJ, Pilhofer M, Weiss GL, Hadfield MG, Jensen GJ, & Newman DK (2014). Marine tubeworm metamorphosis induced by arrays of bacterial phage tail-like structures. Science (New York, N.Y.), 343 (6170), 529-33 PMID: 24407482

April 17, 2014

Terms of Biology – Syntrophy

by Elio

Figure1 Figure 1. An example of syntrophy. Here, benzoate degradation is carried out by a model syntrophic consortium. Dashed blues lines indicate additional sources of cell carbon for the methanogens. Source.

Syntrophy or “eating together” is a kind of symbiosis widespread in biology and of great importance for key biochemical transactions on this planet. Indeed, the cycling of carbon in many of its aspects depends on microbial syntrophy. Thus, the breakdown of waste material critically depends on chemical modifications brought about by microbial syntrophic associations. The phenomenon basically, requires reverse electron transfer, i. e., the input of energy to drive critical redox reactions.

The term syntrophy was first used in microbiology to describe the association between chemotrophic sulfate reducing and phototrophic sulfur oxidizing bacteria. Syntrophy exists between two species of bacteria, two of archaea, or one of each. Lucky for us, a fine essay on this subject was written a few years ago by McInerney, Sieber, and Gunsalus. A later, more detailed review by the same authors is found here, and by others here as well. You will encounter a large variety of fascinating syntrophic associations as well as learning of the ingenious ways that microbes have evolved to squeeze out the last drop of energy from thermodynamically unfavorable reactions. A classic example of symbiotic syntrophy involves an archaeon that can convert methane into CO2 and hydrogen by virtue of a sulfate-reducing bacterium siphoning off the hydrogen byoxidizing into into H2S. And more complex systems abound. For instance, in a tripartite relationship, bacteria in anaerobic environments degrade polymers into acetate, long chain fatty acids, and other compounds, other microbes convert these into hydrogen, formate, and acetate, and a third group use these to make methane and CO2.

The authors pose the question of how do syntrophic cell partners communicate? The answers are not obvious and require further investigation. But a great deal is known already. In the authors’ words: Genomic analysis has revealed the genetic blueprints of model syntrophic substrate-utilizing microorganisms, which in turn has provided insights into the metabolic pathways operative for carbon and electron flow to the end products acetate, hydrogen, and formate. The emerging bio- chemical paradigm includes the need for reverse electron transfer via membrane-bound as well as cytoplasmic confurcation-type enzymes that dispose of electrons as hydrogen and/or formate. Syntrophic strategies truly exist at the thermodynamic limits of life."

March 24, 2014

Six to Tango

by Elio

Something There Is That Likes Symbioses

Figure1 Figure 1.

One genome at a time can be exciting, but two even more so. I’m not entirely sure why this is, although it may explain our fascination with sex. And what if more than two entities were involved? What if the intimacy were not just between two individual organisms, but between a greater number of different ones? Not merely a happy couple, not even limited to a ménage à trois, but an exuberant symbiotic orgy? What could be lovelier?

High on the list of symbiotic wonders are the sap-sucking insects (aphids, mealybugs, psyllids) and their bacterial endosymbionts. The partners appear to have evolved together and to have established a harmonious coexistence eons ago (see Fig. 1). This follows from the fact that plant sap is essentially a sugar solution, so if that’s all an insect eats, how does it get the amino acids, vitamins, and other essential nutrients it cannot make itself? The answer is from the endosymbiotic bacteria it carries within specialized cells in its abdomen called bacteriocytes. These welcome guests provide their host with many—but not always all—the missing nutrients. This theme of “feeding through symbiosis” is repeated up the evolutionary scale, culminating in our phylogenetic neighborhood with the ruminants.

Continue reading "Six to Tango" »

January 13, 2014

How do they make it work? Genomic Revelations on a Bacterial Consortium

by Johnna L. Roose

Figure1 Fig. 1. A Happy Couple. Source.

Do you ever look at a couple and wonder… ‘Why are they together? What does X see in Y. I just don’t get it.  Is X in it only for the money’?  Who doesn’t at times ponder about such matters? There’s practically an entire economy based on it. However, you didn’t find this article while waiting to check out in the grocery line. This post isn’t about celebrities; it’s about microbes.  No matter—some microbe relationships have us scratching our heads and, to the same degree, casting premature judgment.

Fig. 2. Scanning electron micrographs of “Chlorochromatium aggregatum”. (A,B) Epibionts are shown in false color green, central bacteria in false color purple. (B) The central rod is dividing, and most of the epibiont cells have dissociated from the consortium. Scale bar in (B) equals 1 μm. Source.

Two Heads Beat One

One great example of such a conundrum is represented by the phototrophic consortium Chlorochromatium aggregatum, (this invalid name derives from an ancient era, when it was thought to be a single organism). In fact this is an unusually sophisticated prokaryotic symbiosis between a central motile heterotroph (Candidatus Symbiobacter mobilis) surrounded by multiple epibiont cells of a photoautotrophic green sulfur bacterium (Chlorobium chlorochromatii) (Figure 1). At first glance, this seems like a reasonable pairing, to combine mobility with photosynthetic autotrophy for the benefit of both organisms. Taking a deeper look at this relationship raises more questions. According to Don Bryant, "The relationship of these organisms is that of a highly dysfunctional marriage between a workaholic/nitrogen fixer/primary producer that is strictly anaerobic, and an oxygen-requiring, stressed-out, addicted soccer person that provides the bus, the driver and the GPS system.” Thus, in the microbial world as elsewhere, relationships are more complicated than they seem to be.

To gain insights as to how these organisms make this tryst work, researchers have, not surprisingly, turned to genomics for answers. In Genome Biology, Liu and co-authors report the complete genome sequences of both Chl. chlorochromatii and Ca. S. mobilis (Figure 2).  They uncovered plenty of interesting details on the intimate relationship between these two organisms.

Continue reading "How do they make it work? Genomic Revelations on a Bacterial Consortium" »

September 26, 2013

Who Would Have Thought? Biggest Flower, Biggest Gene Thief

by Elio

Rafflesias in the tropical rain forests of Southeast Asia produce some of the biggest flowers in the world—up to one meter in diameter. Adding to their notoriety is their carrion-like smell to attract insects for pollination service. They’re not microbes by anyone's definition of the term. The reason they make an appearance in these pages is that they have stolen a larger proportion of their genome via horizontal gene transfer (HGT) than any other organism we know of. Between 24% and 41% of their mitochondrial DNA is of foreign origin, and even in their nucleus a whopping 2.1% of the genes were imported.


Fully opened flower of Rafflesia arnoldii from the Palupu
Reserve near Bukittinggi, Indonesia. Photo by Troy Davis.

Plant genomes seem to be especially rife in genes acquired by HGT, and this is particularly true for the parasitic kinds, of which the Rafflesias are impressive examples. These freeloaders have no leaves or stems, no plastids anywhere—thus no photosynthesis. They live off host vines whose nutrients they harvest via haustoria, absorptive organs that penetrate into the host’s tissues. These un-plantlike plants exist concealed within their host vines, only occasionally offering a showy reproductive structure to the outer world—reminiscent of the mushrooms formed by underground fungal mycelia. Now we have learned that they are not only trophic parasites, but also genomic thieves.

Continue reading "Who Would Have Thought? Biggest Flower, Biggest Gene Thief" »

August 26, 2013

Mycorrhizal Fungi: The World’s Biggest Drinking Straws And Largest Unseen Communication System

by Elio

Figure 1. Mycorrhizal fungal filaments around a plant root. Source.

Quick, which is the biggest symbiotic association on Earth? Did you guess the mycorrhizae? They are the huge symbioses between fungi and the roots of most terrestrial plants. Their total size is not easy to measure because not all the fungal filaments in soils are mycorrhizal nor are the mycorrhizal ones always mycorrhizing (a new verb?). Even so, one can make the case that the combined mass of the participating fungi and plant roots is colossal. A friend, the soil microbiologist David Lipson, tells me that the mass of mycorrhizal fungi on the planet is estimated to be somewhere around 1-3 x 1010 tons (that’s between 1.4 and 4 tons per person). We are obviously talking about a topic that deserves much more of our attention than it has received to date.

Plants depend on mycorrhizal fungal filaments to supply them with a stunning proportion of their needed water and minerals. In some forests, these fungi provide the plants with up to 80% of their nitrogen and 90% of their phosphorus. The fungi, in turn, depend on plants to provide them with organic compounds needed for their own growth. Although it had been stated that this traffic in carbon is unidirectional—plants-to-fungi—some 400 species of non-photosynthetic plants (e.g., Indian pipes) that lack chlorophyll are proof to the contrary. For these mycoheterotrophs, mycorrhizae are the primary suppliers of essential carbon compounds.

Continue reading "Mycorrhizal Fungi: The World’s Biggest Drinking Straws And Largest Unseen Communication System" »

July 29, 2013

Fine Reading: The Second Skin – Ecological Role Of Epibiotic Biofilms On Marine Organisms

by Elio

In contrast to air, the ocean represents a benign environment for most living organisms: With the exception of some harsh marine environments, the means of physicochemical properties are generally not far off the optimum of most species and their fluctuations are moderate, rarely exceeding biological tolerance limits. So begins a review by Wahl and colleagues on the virtues of marine waters as a habitat. I can’t say that I had given this much thought. Anticipating interesting insights, I read on: As a consequence, insulating coatings of the epidermis such as hair, feathers, wax are not required in the marine realm. No big surprises there, but the implications of it, as explored by these authors, are vast and far-reaching.

Figure 1. Biofouling coating test. 12 x 12 inch test panels exposed at the intake of a power plant for 1 year. Some of these panels were uncoated controls, others were coated with various nontoxic compounds intended to inhibit biological fouling. Minor benefits, if any, can be attributed to the coatings. Score: 1 for nature, 0 for coatings! Source.

Lacking such protective barriers, the body surfaces of marine organisms more intimately engage with the environment and participate in actively acquiring essential nutrients, gases, light, and information. Bathed continually in seawater, these surfaces invite colonization by microbial biofilms, a “second skin.” Such living coverings tend to be thicker and more permanent among aquatic organisms than terrestrial ones (especially if you take a shower every day). While such biofilms can be essential partners, the wrong participants or excessive growth can be detrimental, leading, for instance, to fouling. We associate 'fouling' with biofilms that interfere with our activities, such as the communities that form on the hulls of ships, on membranes in desalination plants, or on catheters. But fish, algae, and other ocean dwellers also are beset by fouling that can reduce exchanges with their environment, alter buoyancy, impede motility, influence feeding, or even interfere with mating. Numerous factors come into play to influence the density of the epibionts colonizing animals and algae.

Continue reading "Fine Reading: The Second Skin – Ecological Role Of Epibiotic Biofilms On Marine Organisms" »

July 08, 2013

Let There Be Light!

by S. Marvin Friedman

As discussed in a recent epic Perspective on the animal-microbe symbioses (and commented in this blog), we are beginning to understand the many contributions made by each partner. One of the most widely studied symbioses is that of the luminous bacterium Vibrio fischeri and the Hawaiian Bobtail squid, Euprymna scolopes. In a recent publication, Heath-Heckman and coworkers determined that bacterial bioluminescence regulates the expression of a squid circadian rhythm (cryptochrome) gene (cryptochromes are a family of blue light receptor proteins involved in circadian rhythms of animals and plants).

Fig. 1: The Hawaiian Bobtail Squid. Credit: Source.

Over the past few years, bacterial partners have been implicated in their host’s circadian rhythms. For example, in humans, immune competence requires that such rhythms be intact. Normal functions of the gut, such as peristaltic activity, undergo circadian rhythms that are likely to be impacted by the gut microbiota. Likewise, several conditions, such as obesity, diabetes, depression, and sleep disorders are associated with aberrant circadian rhythms and imbalances in the gut microbiota. Tantalizing though this is, in none of these systems has a direct interaction between symbiont and host been demonstrated. The first instance involves the squid and its vibrio.

Continue reading "Let There Be Light!" »

June 13, 2013

Fine Reading: The gut microbiota of insects – diversity in structure and function

by Elio

Now that the mammalian intestinal microbiome has been promoted to organ status, might not such stately respectability be granted to the gut microbiota of other metazoans? If looking for a worthy candidate for such recognition, one could not do better than to consider the varied communities dwelling in the guts of insects. A recent review by Engel and Moran points out that beneficial intestinal microbes here: upgrade nutrient-poor diets, aid digestion of recalcitrant food components, protect from predators, parasites and pathogens, contribute to inter- and intraspecific communication, affect efficiency as disease vectors, and govern mating and reproductive systems. Microbes, it is clear, have contributed mightily to insect success.

A. Generalized gut structure of insects. The foregut and hindgut are lined by a cuticle layer (black line), the midgut secretes a peritrophic matrix (dashed line). B-M: Gut structures of insects from different orders. If not specifically indicated, the gut of an adult insect is shown. Stipples depict the predominant localization of the gut bacteria. For plataspid stinkbug, the magnification shows bacteria localized in the midgut crypts. Source.

The microbial landscape of the insect gut microbiome is much different from that of mammals. The great diversity of insects is reflected in their digestive tracts that also differ greatly in anatomy and physiology, and thus accommodate microbiotas that vary in composition and number. The total number of bacteria present range from 109 per honey bee, to 105 in a fruit fly, to negligible numbers in the sap-feeders, the latter often carrying instead an abundance of bacterial endosymbionts. Pick any individual insect and likely it will have fewer species in its gut than you do, although there are exceptions. Perhaps the most diverse communities among the insects are those in the termites, which are teeming with bacteria and protists. The 19th century American paleontologist and biologist Joseph Leidy observed that when one ruptures the intestine of a termite, myriads of the living occupants escape, reminding one of the turning out of a multitude of persons from the door of a crowded meeting-house.

Continue reading "Fine Reading: The gut microbiota of insects – diversity in structure and function" »

May 27, 2013

Stuck in Phage Heaven

by Merry Youle

Fig 1 stuck in heaven
Figure 1. This image, intended to highlight the mechanism of the DNA packaging motor of phage T4, also provides a vivid representation of the 155 Hoc proteins (yellow) assembled into the capsid with their Ig-like domains extending outward. Green = major capsid protein; purple = vertex protein; blue = outer capsid proteins Soc; yellow = outer capsid protein Hoc. Source.

Ceteris paribus, the more prey, the better the hunting. The successful fisherman fishes where the fish are, the skillful pride of lions hunts where the wildebeest gather, and savvy phage predators hang out where the bacteria are. Such bacteria-rich locations include the protective mucus layer formed by animals to protect their vulnerable exposed surfaces. Bacteria—symbionts and pathogens alike—find mucus hospitable; it offers them food and a structured environment. The congregation of bacteria makes mucus a good place for phages to hunt their prey, and some have evolved to exploit this resource. Thus, while looking after their own interests, phages here also serve as an antimicrobial defense for their metazoan host.

The rule of thumb is that phage virions outnumber bacteria in most environments by roughly ten-to-one. Barr et al. recently reported that this ratio is increased more than four-fold in mucus sampled from a wide range of metazoans, from corals to humans. Unlike chemotactic bacteria, phages can’t actively move towards mucus. That there are more phages in mucus than in the adjacent milieu implies that when good fortune and diffusion brings them to the mucus layer, they adhere and stick around. The obvious question is how.

Continue reading "Stuck in Phage Heaven" »

Teachers' Corner


How to Interact with This Blog

  • We welcome readers to answer queries and comment on our musings. To leave a comment or view others, remarks, click the "Comments" link in red following each blog post. We also occasionally publish guest blog posts from microbiologists, students, and others with a relevant story to share. If you are interested in authoring an article, please email us at elios179 at gmail dot com.

Subscribe via email



MicrobeWorld News