A River’s Microbiome May Protect Wild Salmon Against Malnutrition

Chinook salmon may be canaries in the coal mine by revealing that widespread thiamine deficiency could be quietly chiseling away at fish, bird and wildlife populations across the northern hemisphere

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Thiamine, also known as vitamin B1, is an essential dietary cofactor that is critical to proper cellular function in all living beings, playing a critical role in converting food into energy. Without enough thiamine, cellular-level functioning begins to fail. Affected animals behave abnormally, suffer immunosuppression, neurological and reproductive disorders, and can eventually die. Thiamine deficiency disorders can potentially reduce populations of affected species.

Thiamine deficiency complex (TDC) is known to affect Atlantic salmon in the Baltic Sea. But now, Chinook salmon in California’s Central Valley are also showing signs of TDC. Symptoms of TDC in salmonids are first noticeable between hatching and first feeding, and include abnormal swimming patterns and high mortality rates.

Disturbingly, salmon are not the only wild animals that are developing TDC, although they are amongst the most economically important. TDC is apparently increasing throughout marine ecosystems around the globe, causing deaths in invertebrates, fishes, and birds. For example, in 2009, a study investigated the cause of a peculiar idiopathic (“idiopathic” refers to a disease or condition that either arises spontaneously or that has an unknown cause) paralytic condition affecting birds of more than two dozen species in the Baltic Sea region (ref). In addition to paralysis and other neurological problems, the authors reported that TDC apparently causes female birds to lay fewer eggs and lowers chick survival. They proposed that these breeding failures were related to thiamine deficiency and this form of malnutrition could even be responsible for widespread declines in bird populations (also see ref).

Chinook salmon are native fish species found throughout many freshwater river systems of Western North America, ranging from California to Alaska, as well as northern Japan all the way up to the Palyavaam River in Siberia. Being anadromous, salmon hatch in freshwater rivers and migrate to the ocean where they spend several years (some salmonid species longer than others) before attaining breeding size and age.

But where does thiamine naturally originate? A recently published study by microbiologist Christopher Suffridge, a senior research associate at Oregon State University, and doctoral student Kelly Shannon, sought to answer this question by examining concentrations of thiamine and the microbial communities in rivers of the Sacramento River watershed (Figure 1).

“This study is the first-ever report of thiamine compounds in salmon spawning rivers and the associated gravels where salmon spawn,” study lead author Dr Suffridge said in a statement. “This source of thiamine has potential implications for reducing health impacts on naturally spawning salmon that are suffering from thiamine deficiency complex.”

You may be wondering why salmonids are suddenly becoming thiamine deficient now, after tens of thousands of years of excellent health?

“It’s a complicated issue,” study co-author Mr Shannon replied. “The broader context is that Central Valley Chinook salmon, as well as some populations of salmon in other places, are becoming thiamine deficient because of shifts in their diet in their feeding grounds.”

Historically, Mr Shannon explained, Central Valley Chinook salmon ate a diverse diet consisting of many different species of prey fishes. But since 2015, thanks to climate change, warmer coastal waters along the West Coast have caused populations of the northern anchovy, Engraulis mordax, to explode. Unlike many other species of small “bait fish”, anchovies thrive in warmer water, where they feed on plankton that floats on the surface of the water. Global warming due to increased concentrations of carbon dioxide then increases ocean temperatures that, in turn, further boosts plankton populations. Due to their increased numbers, anchovies have become the primary dietary component for wild salmon, especially those feeding in shallow coastal waters before leaving the Pacific Ocean to enter their fresh water spawning areas.

What is the connection between anchovies and TDC?

“Northern anchovies are high in an enzyme called thiaminase that degrades thiamine,” Mr Shannon replied (Figure 2). “So by the time many California Central Valley Chinook salmon are ready to spawn they have been feeding on so many anchovies that they have become deficient in thiamine from the activity of the thiaminase enzyme in anchovies.”

Apparently, salmon acquire thiamine by ingesting it in their prey, and females pass nutrients to their developing eggs, so this TDC indicates that something is seriously wrong in the Pacific Ocean ecosystem, which is the last place that adult salmon feed before entering fresh water to spawn. Further, female salmon with TDC can pass this dietary deficiency to their hatchlings.

California hatchery employees first began noticing high mortality rates in hatchery fish fry in early 2020, and soon linked these deaths to thiamine deficiencies caused by changes in salmon diet in the Pacific Ocean.

“In California, most hatchery-spawning Chinook salmon are treated with thiamine to prevent TDC,” Dr Suffridge pointed out.

Treatment by placing newly-hatched salmon in a thiamine bath solves the problem in the short term, but these treatments offer long-lasting results, nor it does not address the underlying problem. Thus, the health of young salmon could once again deteriorate after they enter the marine environment where the deficiency seems to arise.

“However, it was previously unknown if there was a source of thiamine in the environment that could potentially rescue naturally spawning salmon afflicted with TDC,” Dr Suffridge observed.

This study finds that microbes in river sediments are the likely source of microbial thiamine, and this could supplement — rescue — early life stages of Chinook salmon that experience TDC.

“We have now identified microbially produced thiamine in natural salmon spawning habitats,” Dr Suffridge said.

“It was unknown if the vitamin could even be measured in rivers in the first place, and the thiamine concentrations we measured were much lower — more than a million times lower — than a hatchery thiamine bath,” Mr Shannon added.

Future studies will examine to what degree environmental thiamine acquired by adult Chinook salmon, their incubating eggs and hatched fry could alleviate the negative health outcomes caused by TDC. But this does not identify the deeper cause for this worrying problem. For example, could an environmental shift have somehow slowed or stopped thiamine production, or impeded its movement through the food web? How many species are affected? Is the problem getting worse? And if humans caused the problem, can we reverse it?

“The data have implications for salmon health but are not concrete enough to say anything definitive,” Mr Shannon said. “More research is needed to determine what role the environmental thiamine might play, but obviously learning that it’s there is an important first step.”

Source:

Christopher P. Suffridge, Kelly C. Shannon, H. Matthews, R. C. Johnson, C. Jeffres, N. Mantua, A. E. Ward, E. Holmes, J. Kindopp, M. Aidoo, F. S. Colwell (2023). Connecting thiamine availability to the microbial community composition in Chinook salmon spawning habitats of the Sacramento River basin, Applied and Environmental Microbiology | doi:10.1128/aem.01760-23

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