In Ishiro Honda’s 1954 “Godzilla”, the world is menaced by a towering, semi-aquatic kaiju who wreaks havoc on coastal cities and villages. The monster seems impossible to stop, repelling high-powered military artillery and stomping on tanks. However, Emiko Yamane (played by Momoko Kochi) stumbles on a new weapon which seems to arrest all life in water, called the “Oxygen Destroyer”. This device robs all oxygen from marine life, suffocating anything nearby. As a last resort, the Oxygen Destroyer is deployed while Godzilla is asleep on the bottom of the ocean; he is consequently killed… or is he?
For over 7 years the lab has worked to try and understand the etiology of sea star wasting disease, which is the most geographic extensive marine mortality event ever observed. Since the fall of 2013 the condition has affected over 20 different species of sea star, some more intensely than others. The precipitous decline in the sunflower star even led to its listing on the IUCN Red List, which draws attention to its conservation status as an endangered species. The condition affected sea stars, at different times, from the Gulf of Alaska to Baja California, and similar conditions have been reported in Australia and along the Chinese coast of Shandong in the Yellow Sea. The dramatic collapse of these iconic marine animals, many species of which perform keystone roles in the ecosystem, has attracted considerable attention of citizen scientists, the popular media, and scientists alike.
Yet, the mechanisms underlying sea star wasting have remained elusive. In late 2013 through 2014, my lab pursued viruses as a potential infectious agent – certainly, the patterns of wasting occurrence and apparent transmission between habitats and into public aquariums suggested some form of transmissible agent. We had just completed work on the first described viral group in echinoderms, called densoviruses, when emails circulated about sea star mass mortality. We examined viruses that inhabited infected animals and compared them to healthy specimens across many species and between sites using a relatively novel approach known as viral metagenomics. Nothing stood out as uniquely associated with dying animals, but densoviruses were the best candidate group occurring across all species and seemed somewhat pronounced in dying individual specimens. Following some targeted molecular approaches, and work done by collaborators which showed that tissues that were homogenized and filtered to exclude larger microorganisms and tissues, we concluded that the sea star associated densovirus was the closest thing to an agent associated with the condition – a candidate agent in science-speak.
But something didn’t add up in this story. We tried, unsuccessfully to replicate the early experiments many times to no avail; we found lots of the sea star associated densovirus in perfectly healthy specimens, and none in rotting individuals. We looked at other viruses, bacteria, and other microorganisms in more detail to see if any were associated with wasting, but none were. In fact, for a couple of years we had a very difficult time getting sea stars to waste at all – and when we didn’t try through experiments, they wasted on their own. We also noticed, at about this same time, that sea star associated densovirus wasn’t in isolation within sea star tissues; there were many different close relatives; redesigning our targeted molecular approaches revealed no association between this virus and the condition. What’s more, we didn’t see any virus through several further studies – so it was back to square one.
Further work by colleagues suggested that maybe the condition was associated with unusual warm weather events – known as heat waves. This inspired us to look at oceanographic data on water temperature as it varied during mass mortality, and even looked at precipitation patterns as a kind of proxy for rainfall in the region. 2013-2014 marked significant drought on land adjacent to wasting, but the mechanism for how this might affect sea stars wasn’t clear. The most promising correlate based on our work was drastic shifts in temperature (from warm, to cold, then back to warm) over short periods, which appeared to correspond with mass mortality onset when it occurred. Taking this cue, and after several years of zero wasting observation during experiments, we set out to test whether swinging temperatures could generate disease. We collected specimens from a field site in central California, and kept them in a common garden for a few weeks. Unexpectedly, they developed lesions without any additional stimuli. This was the first time we’d seen wasting in any experiment for a few years! But this happened without any temperature swing, so despite the good news this sent us back to square one again. We designed additional experiments to see whether desiccation (warm summer days and low humidity?), water replacement (more stable water column condtions?), abrasion (physical damage on collection?) or protein-bearing material caused wasting – it was at that stage a bit of an open book. To our surprise, once again, everything caused wasting compared to controls. Somewhat discouraged, we decided to look at what happened to the microbiomes and viromes of sea stars as they went from completely healthy to being carcasses in the hope that this would shed light on potential pathogens.
Revisiting our work on viruses, we looked at what types of viruses infected tissues as animals wasted, and saw nothing distinct to wasting sea stars; this confirmed that sea star associated densovirus, at least from an association standpoint, could not be associated with sea star wasting disease. Looking at bacterial microbiomes provided a significant clue for wasting disease, and one that we hadn’t expected. While not a perfect correlation, bacteria which thrived in low or no oxygen environments seemed to appear immediately before or at the time that lesions on the animals appeared. Normally seawater is replete with oxygen – so how could anaerobes persist and proliferate? Looking at other types of bacteria, it seemed that several genera and species of bacteria which thrive on high organic matter, called copiotrophs, seemed to increase in abundance before the animals developed lesions. Normally sea stars put out a bunch of highly usable (called labile) organic matter, so this was not unexpected. However, these observations stimulated the idea that perhaps wasting disease was somehow related to microbial activities at the interface between animal tissues and overlying waters. But why would this happen? Bacteria normally thrive on organic matter not only excreted from animals, but also by matter that is excreted by phytoplankton and other primary producers, excreta of zooplankton, and decaying carcasses of animals. Looking at trends in primary productivity at a field site at which sea star wasting was also monitored, it became clear that sea star wasting occurred annually when phytoplankton abundance was maximum or immediately after, oxygen concentrations were lowest, and temperature was greatest. These observations and surveys generated a new hypothesis: bacterial activity at the animal-water interface, stimulated by organic matter from phytoplankton or other algal material or possibly by decaying animal tissues (which would be present in tissue homogenates) may lead to suboxic microzones at the animal-water interface; this may in turn affect the animal’s ability to maintain their tissues, repair wounds, and fend off invading microorganisms through breaches in their tissues.
So, in 2019 we pursued additional experiments to directly test these; we incubated sea stars in aquaria where oxygen was depleted and compared them to fully oxygenated controls; almost all treated animals developed lesions and died, whereas those in controls stayed healthy throughout our experiment. We then tested whether organic matter, when added directly to sea stars, could generate wasting. We chose two amendments mimicking our hypothesized phytoplankton-OM link to wasting (an algal culture and naturally collected phytoplankton), and something that we knew would stimulate most marine bacteria (peptone). Most organic matter addition caused SSWD, and furthermore led to changes in their microbiomes which were consistent with what we saw in the earlier survey monitoring sea stars that wasted without any additional stimulus. We took this as proof that wasting was indeed related to microbial activity occurring at the animal-water interface.
But lingering questions remained, notably: Why were some species more heavily affected than others? And was this effect at work in 2013-2014 during mass mortality? To answer the first question we asked whether there were physical differences in the sea stars which may cause more extensive layers of still water to occur on their surfaces. We examined this using computed tomography, which showed that more heavily affected species were rougher (and therefore had a much larger boundary layer (the layer at the animal-water interface) than those species which were less affected. Because we didn’t have specimens from 2013-2014 that were amenable to molecular work (due to several freezer failures), we instead looked for signals of anaerobic processes in affected specimens from the time (compared to healthy ones) using stable isotopes. Certain elements become enriched under anaerobic conditions; indeed, specimens in anaerobic conditions had greater amounts of these signals than healthy specimens collected at the same time.
The results of this work have important implications. Normally the word “disease” is synonymous with some kind of infectious agent, be it a virus, bacterium or other microbe. Our work, however, suggests that sea star wasting was caused by non-pathogenic microorganisms living near, but not within, sea stars. It also suggests that there may be diseases in marine habitats that may look like they’re being transmitted from one individual to another, but in fact may be via transfer of organic matter from dying or decaying individuals to healthy individuals.
There are still alternate explanations for sea star wasting disease etiology – for example, could the organic matter that is released from dying stars be some kind or hormone or other molecule (organic in nature) that told healthy stars to die? Or could the sheer presence of high bacterial activity on animal surfaces result in some kind of inflammation which ultimately leads to wasting? And what on earth was the sea star associated densovirus doing to stars if not causing significant disease? All these questions will hopefully be answered by other researchers in the future.
So, Ishiro Honda may have been correct in his sci-fi classic. While no kaiju, sea stars are monsters in their world – but important monsters they are. And instead of a weapon like an “oxygen destroyer”, these monsters may be taken down by natural processes that are made worse during extreme weather and climate change. We’ve learned a lot from this work, and hope that future research by others will continue to critically examine whether marine disease events are truly infectious in nature, or whether it is processes that occur at spatial scales difficult to measure using conventional approaches an instrumentation that are at play.
You can read more about our work at this link.